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BOTRYOTINIA 
AND 

BOTRYTIS 
SPECIES: 



laxui lui I ly ^ 
physiology and 
pathogenicity 



Monograph No. 15 

1977 



■ ^1^ Agriculture 



Canada 



BOTRVOTINIA 
AND BOTRYTIS 
SPECIES: 

taxonomy, physiology, 
and pathogenicity 

A guide to the literature 



W. R. Jarvis 

Research Station 

Harrow, Ontario NOR IGO 



Research Branch 

Canada Department of Agricuhure 



Monograph No. 15 
1977 



Copies of this publication may be obtained from 

INFORMATION DIVISION 

CANADA DEPARTMENT OF AGRICULTURE 

OTTAWA 

KIA 0C7 

©MINISTER OF SUPPLY AND SERVICES CANADA 1977 



2M-38745-7.77 
Cat. No.: A54-3/15 
ISBN No.: D-662-00794-8 

Hignell Printing Limited 
Contract No.: 0KT7-1078 



i 



CONTENTS 



PART 1 Introduction 9 

PART 2 Taxonomy 11 

Taxonomic review 11 

Sclerotiniaceae 11 

Botryotinia 12 

Botryotinia and Botrytis 13 

Botrytis 14 

The basis for classification 16 

Numerical taxonomy 17 

Biochemical differentiation 18 

Variability 18 

Sexual reproduction 18 

PART 3 Form and Function 20 

Anatomy and morphology 20 

Mycelium 20 

Conidiophores and conidia 20 

Microconidia 21 

Chlamydospores 22 

Oidia 22 

Haustoria 22 

Appressoria 23 

Organs of attachment 23 

Sclerotia 23 

Apothecia 25 

Ultrastructure 25 

Cytology 27 

Variants 29 

Adaptation to fungicides 31 

Growth 33 

Effects of temperature 33 

Effects of relative humidity 34 

Effects of light 35 

Phototropism 38 

Effects of pH 39 

Effects of age and nutrition 39 

Staling 41 

Effects of volatile metabolites 42 

Effects of atmospheric gases and pollutants 42 

Autotropism 44 

Rheotropism 44 

Sporulation inhibitors 45 

Storage 45 

3 



Metabolism 46 

Selective media 46 

Carbohydrates 46 

Nitrogen 48 

Amino acids and proteins 49 

Aliphatic compounds 50 

Vitamins 51 

Trace elements 51 

Alkaloids 51 

Pigment production 52 

Hydrolytic enzymes 52 

Polyphenols 52 

Test organisms 53 

Survival 53 

Dispersal 57 

PART 4 Pathology 62 

Host specificity 62 

Infection 64 

Infection from conidia 64 

Infection from microconidia 69 

Infection from mycelium 69 

Infection from ascospores 69 

Inf ectivity 70 

Predisposition 72 

Moribund tissue 72 

Frost 73 

Wounds 73 

Water status 74 

Exosmosis 75 

Volatile metabolites 76 

Carbohydrate status 77 

Nitrogen 79 

Light 79 

Microorganisms 80 

Pollen 80 

Fertilizers 81 

Pathogenesis 82 

Enzymes 83 

Toxins 84 

Restricted lesions 86 

Osmotic relations 88 

Effects on host metabolism 88 

Resistance 89 

Mechanical resistance 89 

Wound reactions 90 

Immunity 91 

Chemical resistance 92 

Phytoalexins 1 00 



I 



Quiescent infections 102 

Latency 104 

Implications of quiescence in disease control 107 

Disease escape 108 

Epidemiology Ill 

Forecasting 113 

Interaction with other microorganisms 114 

Enology 116 

Principles of control 118 

Fungicides 119 

Storage diseases 119 

Disease escape 119 

Breeding for resistance 120 

PARTS References 121 

APPENDIX Additional literature 181 



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Preface 

The literature on the taxonomy and biology of Botrytis spp., the diseases 
they cause, and their control is vast and I have covered only a small part of 
it here. I have selected for annotation what I consider to be the more informa- 
tive papers that give leads into one or more of several fields. Others, no less 
important but not discussed here, are listed in an appendix in such a way as 
to link them with a computer-filed bibliography on the genus (Jarvis and 
Topham: Bull. Br. Mycol. Soc. 8: 37. 1974). The appendix also includes 
papers inadvertently omitted from this review and those that appeared after 
the text had been completed in December 1974. 

The ever-changing spectrum of fungicide usage has discouraged me from 
compiling a list of all the fungicides ever used against Botrytis spp. and the 
results of their trials; instead, I have concentrated on the principles under- 
lying control measures of all sorts, and simply listed a few reviews giving 
leads to detailed papers that should be consulted, together with Review of 
Plant Pathology and the American Phytopathological Society's annual Results 
of Fungicide and Nematicide Tests. 

I am indebted to Professor John Webster and the late Professor William 
Brown, who introduced me to the rich field of Botrytis biology, to the many 
mycologists and plant pathologists throughout the world, especially those of 
the European Botrytis group, with whom I have discussed the genus, and 
to the many people in Scotland and Canada who have assisted me in the 
production of this review. 



PARTI INTRODUCTION 



Botryotinia and Botrytis species are among the most ubiquitous and 
catholic plant pathogens and saprophytes. They are particularly important on: 

• grape {Vitis vinifera L.) and other Vitis spp. (Bouard, Bulit, Lafon, and 
Roussel 1970) 

• small fruits (strawberries, raspberries, blueberries, cranberries, gooseber- 
ries, and currants) 

• vegetables (lettuce, tomatoes, cucumbers, peas, beans, and peppers) 

• bulbous monocotyledons (onions and other Allium spp. and ornamental 
members of the Liliaceae, Amaryllidaceae, and Iridaceae) 

• forest tree seedlings 

• glasshouse crops (tomatoes, cucumbers, and ornamental crops) (McClellan 
1964; Cramer 1967) 

In the U.K. Moore (1959) lists 13 species of Botrytis in addition to 
B. cinerea on 5 cereal hosts, 4 root and fodder crops, 6 pulse and forage 
crops, 15 vegetable crops, 14 fruit crops, 6 tree species, 58 ornamental hosts, 
as well as on potato, hops, and flax. 

Botrytis spp., and especially B. cinerea, are important pathogens of 
stored and transported fruits, vegetables, ornamental crops, and nursery stock 
(Harvey and Pentzer 1960; Haas and Wennemuth 1962; Smith 1962; Eckert 
and Sommer 1967; Lutz and Hardenburg 1968; Redit 1969; and Coursey and 
Booth 1972). Probably most rots that occur in stored products begin in the 
field and escape detection because many of these infections are latent (q.v.). 
They may develop only when special postharvest conditions of host physiol- 
ogy and the storage environment disturb the equilibrium between the quiescent 
fungus and its host. Their control depends as much on preharvest as on post- 
harvest measures (Smith 1962; Jarvis 1965; and Eckert and Sommer 1967). 

Botrytis cinerea sensu lato and perhaps also sensu stricto has a very wide 
host range; MacFarlane (1968), for example, lists 235 hosts from records in 
the Review of Applied Mycology, Anderson (1924) more than 100 hosts from 
Alaska including 3 genera of Pteridophytes and a species of the Bryophyte 
Lunularia, Baker (1946) 36 hosts, mostly ornamental crops from California, 
Heald & Dana (1924) 20 hosts from Washington, Dingley (1969) 69 hosts 
from New Zealand, and Conners (1967) lists 163 hosts in Alaska, Canada, 
and Greenland from the Canadian Plant Disease Survey. 

Species of Botryotinia with a conidial state of the Botrytis cinerea type 
also include specialized parasites such as Botryotinia convoluta on Iris spp., 
B. ficariarum on Ficaria verna Huds., B. ranunculi on Ranunculus septen- 
trionalis Poir., and B. narcissicola on Narcissus spp. 



Other Botrytis spp. also have a much more restricted host range. Of 25 
species of Botrytis recognized by Hennebert (1963), 14 occurred on species 
in the Liliaceae, Amaryllidaceae, and Iridiceae, 7 on Allium spp., and at least 
6 of them were pathogenic to A. cepa. B. allii (B. aclada) occurred on 4 
Allium spp. On the other hand, A. ursinum was host to only B. globosa, 
(although this species also occurred on A. cepa), A. vineale host only to 
B. porri (also on A. cepa, A. sativum, and A. ascalonicum), and A. triquetrum 
host only to B. sphaerosperma (which itself occurred on no other Allium 
host, though Hennebert (1969) later found it on Lilium regale). 

It is interesting, phylogenetically, to note that the most restricted host- 
specificity in the genus occurs on members of the monocotyledonous division 
Corolliferae and the arguably related dicotyledonous Ranunculaceae. 

Geographically, Botryotinia and Botrytis spp. occur wherever their host 
crops are grown, ranging from cool temperate zones of Alaska (Anderson 
1924), Canada and Greenland (Conners 1967), and Lithuania (Shidla 1971a, 
1971^) to subtropical areas like Egypt (El-Helaly, Elarosi, Assawah, and 
Kilani 1962) and northern New Zealand (Dingley 1969). However, because 
of the distribution of economic hosts, most records are from cool-temperate 
and warm-temperate zones, although B. cinerea often occurs as a snow mold, 
especially in forest nurseries (Sato, Shoji, and Ota 1959). Most species occur 
in all continents, but Botryotinia ranunculi is recorded only in North America 
and B. ficariarum only in Europe; B. calthae (also from the Ranunculaceae) 
is recorded from both continents (Hennebert and Groves 1963). None of these 
are known in other continents. 

Botrytis spp. are not usually regarded as soil inhabitants (Park 1955) but 
rather as ephemeral mycelia associated with decaying plant residues (Domsch 
and Gams 1972; Scurti, Fiussello, and Jodice 1972), probably degrading 
cellulose (Janke 1949; Franz and Loub 1959; Niethammer, Krehl-Nieflfer, 
and Hitzler 1959; and Domsch 1960), pectin (Loub 1960; Nyeste 1960; and 
Domsch and Gams 1969), cutin (Linskens and Haage 1963), and araban 
(Kaji, Tagawa, and Motoyama 1965), but not xylan (Domsch and Gams 
1969). Botrytis cinerea and a Botrytis sp. were readily isolated from soils by 
immersion tubes and screened immersion plates by Chesters and Thornton 
(1956). Luppi-Mosca (1960) isolated B. cinerea from depths of 40-60 cm 
in a forest soil. 

Barron (1968) thought that although B. cinerea may be relatively com- 
mon in soil, it sporulates poorly there and is underestimated by normal tech- 
niques such as dilution plates. Lockwood (1960) and Hsu and Lockwood 
(1971) considered it only a moderately good competitor in soil, surviving as 
mycelium for less than 2 wk. Lorbeer and Tichelaar (1970) devised a selec- 
tive medium for the isolation of B. allii (B. aclada) from soils and recovered 
it successfully from the sandy soils of the Netherlands and the organic soils 
of New York. 

The position of B. cinerea in the ecological succession of fungi on plant 
remains above the soil was considered by Hudson (1968). 

10 



PART 2 TAXONOMY 



TAXONOMIC REVIEW 



In the most recent review of Discomycete taxonomy (Korf 1973), 
Botryotinia Whetzel (1945) is placed in the order Helotiales and the family 
Sclerotiniaceae Whetzel (1945). 

The form-genus Botrytis Pers. is placed by Hennebert (1973) in the 
Hyphomycete family Botrytidaceae Lindley and in Hughes' (1953) conidio- 
genetic section IB; the conidiophores are straight, are branched alternately, 
and they proliferate; the conidia are usually one-celled, gray to brown, 
globose to ovoid, and, in Barron's (1968) classification, botryoblastospores. 

For many years, the diseases caused by Botryotinia and Botrytis spp. 
were confused with those caused by aconidial Sclerotinia spp., especially S. 
sclerotiorum and S. minor, and the confusion extended into taxonomy. Despite 
a clarification by Smith (1900), the confusion persisted (e.g., Zimmermann 
1927) until it was largely dispelled by Whetzel (1945) and Buchwald (1949). 



Sclerotiniaceae 

Whetzel (1945) erected the family Sclerotiniaceae for those Discomycetes 
characterized as follows: apothecium arising from a definite sclerotium or 
stromatized portion of the substratum, stipitate, cupulate, funnel- or saucer- 
shaped (except in Verpd), usually brown; ascus inoperculate, commonly 
8-spored; ascospores ellipsoidal, often flattened on one side, usually hyaline, 
unicellular and smooth; spermatia (microconidia) usually globose to slightly 
ovate; conidial forms various, in most (9 of 15) genera lacking. 

Within the Sclerotiniaceae, Whetzel (1945) used the anatomy of the 
food-storing stroma as an important criterion of relationships among the 
genera. He recognized two generalized types: the sclerotial, of more or less 
characteristic form, and the substratal, of diffuse and indeterminate form. 
Some of the former are formed in aerial mycelium or within host cavities 
and do not replace host tissues, nor contain remnants of them. The tuberoid 
sclerotia of Sclerotinia are of this type. In the discoid sclerotia of Ciborinia 
and the mummoid sclerotia of Ciboria, undigested remnants of host tissues 
are commonly found in the medulla. Noviello (1962) also noted this in a 
Botrytis sp. of the cinerea type that formed sclerotia on leaves of Ficus 
elastica, and Noviello and Korf (1961) reexamined a number of genera for 
the occurrence within sclerotia of cotton fragments when cotton pads, soaked 
in a nutrient broth, were used as substrates. Five species of Botryotinia and 
three of Botrytis had sclerotia containing fragments of the substrate, as had 

11 



Ciborinia and Streptotinia spp., whereas Sclerotinia sclerotiorum, S. trifo- 
liorum, and S. asari ined. had not, and Noviello and Korf concluded that 
Botryotinia and Botrytis were clearly distinct from Sclerotinia and closely 
related to Ciborinia. They also noted that a flexible and gelatinous matrix 
containing hyphae of the medulla was present in sclerotia of Botryotinia, but 
not in Sclerotinia. 

In parentheses it is worth noting that Korf and Dumont (1972) subse- 
quently proposed the transfer of S. sclerotiorum, together with S. tuberosum, 
to a new genus Whetzelinia, distinct from the cypericolous and juncicolous 
species of Myriosclerotinia Buchw., from Sclerotinia { = Ciborinia Whetzel), 
and Botryotinia. 

In the taxonomy of the Sclerotiniaceae, diagnostic features of sterile 
apothecial tissue had mostly been ignored until Korf and Dumont (1968) 
drew attention to their value. Korf (1973) emphasized apothecial and stro- 
matal structure in his review of the taxonomy of the Discomycetes and 
Tuberales. 

Phylogenetic relationships based on sclerotial structure are discussed by 
Willetts (1972), and those based on ascus morphology by Chadefaud (1973). 

Other possible phylogenetic relationships of the Sclerotiniaceae within 
the Helotiales, based on Nannfeldt's (1932) classification of the inoperculate 
Discomycetes, are discussed by Korf (1958). 

The taxonomy of the family was reviewed and revised by Dumont and 
Korf (1971) and by Korf (1973), who gave keys to the orders and genera. 

Some North American and British collections are described by Seaver 
(1951) and Dennis (1968), respectively. 



Botryotinia 

Botryotinia is distinguished from other genera in the Sclerotiniaceae by 
the following characters (Whetzel 1945; Korf 1973): 

stroma a definite black sclerotium, planoconvexoid, characteristically flat- 
tened, loaf-shaped or hemispherical, formed just beneath the host cuticle or 
epidermis and firmly attached; if covered, then eventually erumpent; rind 
poorly developed or lacking on the (flat) attachment surface. 

medulla of slender, thin-walled hyphae, loosely interwoven and embedded 
in a hyaline, flexible to gelatinous matrix, with no interhyphal spaces. 

rind black, distinct, more or less pseudoparenchymatous or palisade-like. 

microconidiophores in a sporodochium, microconidia globose on branching 
microconidiophores, all enclosed in a mucilaginous matrix. 

conidiophores straight, of the genus Botrytis. 
12 



apothecia cupulate and stalked, brown, cup varying from infundibuliform 
to discoid, the margin sometimes reflexed in age. 

ascus inoperculate, J + , clavate. 

ascospores hyaline, unicellular, ellipsoidal. 

appressoria characteristically digitate, formed from mycelial tips in culture 
on glass. 

The type species of Botryotinia is B. convoluta (Drayton) Whetzel 
(1945); it has a Botrytis of the cinerea type as the conidial state. Whetzel also 
included in his new genus Botryotinia porri (van Beyma) Whetzel with 
Botrytis porri as the conidial state, and Botryotinia ricini (Godfrey) Whetzel 
with Botrytis ricini (not of the cinerea type, and subsequently transferred to 
Amphobotrys by Hennebert 1973), as its conidial state. 

Buchwald (1949) made a comprehensive reappraisal of Whetzel's Sclero- 
tiniaceae. He supported the use of the genus Botryotinia (but with B. fuckel- 
iana as the type species) to contain those species with Botrytis conidial states 
and divided it into subgenera. Eubotryotinia subg. n. contained species in 
which the conidial state belonged to the subgenus Eubotrytis (conidia of the 
Botrytis cinerea type) and Sphaerobotryotinia subg. n., in which the conidia 
were globose. Thus, in 1949, Eubotryotinia contained B. fuckeliana (de 
Bary) Whetzel, B. porri (van Beyma) Whetzel, B. convoluta (Drayton) 
Whetzel, and B. narcissicola (Gregory) Buchw.; and Sphaerobotryotinia con- 
tained B. polyblastis (Gregory) Buchw. (type species), B. ricini (Godfrey) 
Buchw., and B. sphaerosperma (Gregory) Buchw. 



Botryotinia and Botrytis 

The connection between Botryotinia (Sclerotinia) spp. and Botrytis spp. 
has been the subject of some controversy, and the situations prevailing up to 
1949 are reviewed by Buchwald. De Bary (1866, 1884, 1886) was convinced 
that Botrytis cinerea and Botryotinia (Peziza) fuckeliana were genetically con- 
nected. In 1864 he named Peziza fuckeliana, but without describing it, as the 
perfect apothecial stage of B. cinerea Pers. and P. fuckeliana was subse- 
quently transferred to Sclerotinia by Fuckel (1869) and to Botryotinia by 
Whetzel (1945). For many years P. fuckeliana remained a nomen nudum 
because of the lack of type material, but Gregory (1949) described slides of 
mounted material from an apothecium, sclerotium, and microconidiophore 
made by de Bary and deposited in the British Museum (Natural History) in 
London and reestablished the validity of de Bary's name. 

By crossing isolates of B. cinerea from Vitis sp. from the Rhine Valley 
(the host and locality of de Bary's collection) with isolates from apple, potato, 
and celery from Canada, Groves and Loveland (1953) obtained apothecia of 
Botryotinia fuckeliana that agreed with de Bary's type material on the slides 
in the British Museum. Thus, they established the genetic connection between 
Botryotinia fuckeliana (de Bary) Whetz. and Botrytis cinerea Pers. 

13 



Botrytis 

The genus Botrytis is one of the first described genera of fungi; Micheli 
erected it in 1729. Persoon (1801) designated five species under the binomial 
system of Linneaus, validated the genus, and included one of Micheli's species, 
B. cinerea, so named by von Haller (1771), in his Synopsis Methodica Fun- 
gorum. By 1822, Persoon had included 27 species and by 1886 Saccardo 
listed 128 species. Many of these were clearly not congeneric and Whetzel 
(1945), Buchwald (1949), and Hennebert (1973) have redefined the genus. 
A comprehensive history of the nomenclature in the genus is given by Buch- 
wald (1949) and Hennebert (1973). The genus Botrytis has accommodated 
a large number of taxa because of misidentifications, because of mistaken 
concepts of the genus as defined by Persoon (1822), and perhaps because of 
some doubt as to the correct type-species. Saccardo (1886), for example, 
divided Botrytis into 4 subgenera on the basis of conidiophore structure: 
Eubotrytis Sacc, Polyactis (Link) Sacc, Phymatotrichum (Bon.) Sacc, and 
Cristulina Sacc; in this system B. cinerea was referred to Polyactis. Other 
genera confused with Botrytis include Beauveria VuilL, Hyphelia Fr., Chro- 
melosporium Corda, and Haplaria Link. Buchwald (1949) emended the 
description of the genus, restricting it to 23 species. Many of the references 
in the literature before 1949 must therefore be treated with some caution. 

Buchwald proposed three new subgenera: (i) the subgenus Eubotrytis, 
having two sections: the Macrosclerotiophorae (large sclerotia) containing the 
species B. porri, B. allii (B. aclada), B. byssoidea, B. squamosa, B. convoluta, 
B. anthophila, B. trifolii, B. cinerea sensu stricto, and B. cinerea sensu lato; 
and the section Microsclerotiophorae (small sclerotia) with the species B. 
tulipae, B. elliptica, B. hyacinthi, B. galanthina, B. narcissicola, B. gladioli, 
B. croci, B. paeoniae, and B. jabae; (ii) the subgenus Sphaerobotrytis , con- 
taining the globose-spored species B. ricini, B. globosa, B. sphaerosperma, 
and B. polyblastis; and (iii) the subgenus Verrubotrytis, containing the single 
species B. geranii. 

The question of the type species had long remained confused. Buchwald 
(1949) was of the opinion that Persoon (1822) had intended B. cinerea to be 
the type species, and himself accepted that the name had also been accepted by 
Fries (1832) in the Sy sterna Mycologicum. Hennebert (1973) evidently con- 
sidered that Clements and Shear (1931) had designated it as the lectotype, 
although they had not discussed the matter. Groves and Loveland (1953), 
however, did discuss it and, apparently overlooking the lectotype of Clements 
and Shear, designated a specimen (on a stem of ? Foeniculum vulgare, Henne- 
bert, unpublished) in the Persoon Herbarium in Leiden as the lectotype. 

Hennebert (1960, 1973) made a comprehensive reappraisal of Botrytis 
and BotrytisAike fungi. Of about 380 taxa assigned over the years to the genus 
Botrytis, he provisionally retained 22 species within his concept of the form- 
genus Botrytis within the family Botrytidaceae Lindley. These 22 species 
are connected with inoperculate Discomycetes of the family Sclerotiniaceae 
Whetzel, in the genus Botryotinia Whetzel. Within the Botrytidaceae, Henne- 

14 



bert (1973) erected 3 other new genera: Streptobtrys n.g., connected with 
Streptotinia Whetzel; Amphobotrys n.g., connected again with Botryotinia, 
and containing one species, A. ricini (Botrytis ricini Buchw); and V errucobo- 
trys n.g., connected with Seaverinia Whetzel and containing one species, V. 
geranii {Botrytis geranii Seaver). A number of other Botrytis-\\\iQ fungi were 
assigned to Dichobotrys n.g., connected with Trichophaea Boudier in the 
family Pyronemataceae Corda; to Chromelosporium Corda, connected with 
Peziza Pers. in the family Pezizaceae Fries; to Pulchromyces n.g. and Phyma- 
totrichopsis n.g., both with no known perfect state; and to Ostracoderma 
Fries and Glischroderma Fuckel, form-genera in the family Glischroderma- 
taceae Rea with no known perfect state. Hennebert published a synoptic key 
to the genera in the same paper, and included the following species in his 
form-genus Botrytis (only valid species have a citation here): 

B. aclada Fresen., Beitr. Mycol. 1:16. 1850 = B. allii Munn 

B. byssoidea Walker in Phytopathology 15: 709. 1925, conidial state of 
Botryotinia allii (Sawada) Yamamoto in Sci. Rep. Hyogo Univ., Ser. Agr. 
Biol. 2:22. 1956 

B. calthae Hennebert in Can. J. Bot. 41: 343. 1963, conidial state of Botryo- 
tinia calthae Hennebert & Elliott in Can. J. Bot. 41 : 343. 1963 

B. cinerea Pers., Syn. meth. Fung. 690. 1801 = Haplaria grisea Link = 
Poly act is vulgaris Link = Phymatotrichum gemellum Bon. = Botrytis fuckel- 
iana Buchw., conidial state of Botryotinia juckeliana (de Bary) Whetzel in 
Mycologia37: 679. 1945 

B. convoluta Whetzel & Drayton in Mycologia 25: 475. 1932, conidial state 
of Botryotinia convoluta (Drayton) Whetzel in Mycologia 37: 679. 1945 

B. croci Cooke & Massee in Cooke in Grevillea 16:6. 1887 

B. elliptica (Berk.) Cooke in Gdnr's Chron. 30: 58. 1901 

B. fabae Sardifia in Mems R. Soc. esp. Hist. nat. 15: 291. 1929 

B. ficariarum Hennebert in Can. J. Bot. 41: 355. 1963, conidial state of 
Botryotinia ficariarum Hennebert in Can. J. Bot. 41: 355. 1963 

B. galanthina (Berk. & Br.) Sacc. Syll. Fung. 4: 136. 1886 

B. gladiolorum Timm. in Meded. Inst. Phytopath. Lab. BloembollOnderz. 
Lisse 67: 15. 1941, conidial state of Botryotinia draytonii (Budd. & Wakef.) 
Seaver in North Am. cup-fungi (Inop.) 62. 1951 

B. globosa Raabe in Hedwigia 78: 71. 1938, conidial state of Botryotinia 
globosa Buchw. in Phytopath. Z. 20: 250. 1953 

B. hyacinthi Westerd. & Beyma in Meded. Phytopath. Lab. W. C. Scholten 
12: 15. 1928 

B. narcissicola Kleb. ex Westerd. & Beyma in Meded. Phytopath. Lab. W. C. 
Scholten 12: 15. 1928, conidial state of Botryotinia narcissicola (Gregory) 
Buchw. in Vet.-og Landboh0jsk. Aarsskr. 1949: 137. 1949 

B. paeoniae Oud. in Vers, gewone Verg. Afd. Natuurk. K. Ned. Akad. Wet. 
1897: 455. 1897 

15 



B. pelargonii Roed in Blyttia 7: 77. 1949. conidial state of Botryotinia pelar- 
gonii R)^ed in Blyttia 7: 77. 1949 

B. polyblastis Dowson in Trans. Br. Mycol. Soc. 13: 102. 1928, conidial state 
of Botryotinia polyblastis (Gregory) Buchw. in K. Vet.-og Landboh0jsk 
Aarsskr. 1949: 137. 1949 

B. porri Buchw. in K. Vet.-og Landboh^jsk. Aarsskr. 1949: 137. 1949, coni- 
dial state of Botryotinia porri (Beyma) Whetzel in Mycologia 37: 680. 1945 

B. ranunculi Hennebert in Can. J. Bot. 41: 348. 1963, conidial state of 
Botryotinia ranunculi Hennebert & Groves in Can. J. Bot. 41 : 348. 1963 

B. sphaerosperma Buchw. in K. Vet.-og Landboh0jsk. Aarsskr. 1949: 137. 
1949, conidial state of Botryotinia sphaerosperma (Gregory) Buchw. in K. 
Vet.-og Landbohgijsk. Aarsskr. 1949: 137. 1949 

B. squamosa Walker in Phytopathology, 15: 710. 1925, conidial state of 
Botryotinia squamosa Viennot-Bourgin in Annls Epiphyt. 4: 38. 1953 

B. tulipae Lind, Danish fungi 650. 1913 = Botrytis parasitica Cavara, sclero- 
tial state of Sclerotium tulipae Lib., = Botrytis tulipae (Lib.) Hopkins 

Hennebert excluded these species, which are frequently encountered in 
early literature: B. carnea, B. crystallina, B. dichotoma, B. epigaea, B. fulva, 
B. luteo-brunnea, B. spectabilis, and B. terrestris. 

Other species that are probably valid, although not yet revised by 
Hennebert, are: 

B. anthophila Bond, in Notes of the Seed-Testing Station, St. Petersburg 1914 

B. convallariae (Kleb.) Ondrej in Biologia (Bratisl.) 27: 23. 1972 

B. spermophila, conidial state of Botryotinia spermophila Noble in Trans. Br. 
Mycol. Soc. 30: 48. 1948 

Doubtful species are B. anacardii, B. artocarpi, B. cana, B. canescens, 
B. douglasii, B. furcata, B. gladioli, B. grisea, B. infestans, B. liliorum, B. lini, 
B. mali, B. plebeja, B. trifolii, B. verrucosa, B. vulgaris, and Botryotinia theae. 

The microconidial (spermatial) state is referred to Myrioconium H. 
Sydow and the sclerotial state to Sclerotium Pers. 



The basis for classification 

Hennebert (1973) adopted Hughes' (1953) system of Hyphomycete classi- 
fication based on conidiogenesis and both placed Botrytis in Hughes' section 
IB, in which the conidia are produced by budding synchronously from 
denticles on a well-differentiated swollen sporogenous cell, the ampulla 
(Klebahn 1930; Whetzel and Drayton 1932; and Hughes 1953). Barron 
(1968) placed it in his series Botryoblastosporae (equivalent to Hughes' 
section IB), which is characterized by the production of botryoblastospores. 

16 



Barron emphasized that the ampulla in the Botryoblastosporae is distinct 
from the similar swelling in some genera of his series Sympodulisporae; the 
ampulla is formed before spore production, not, for example, as the result 
of successive spore formation as in Arthrobotrys spp. 

Botrytis forms part of the Torulaceae of Subramanian (1962) and the 
Blastosporae of Tubaki (1963). In Ellis' (1971) terminology, the conidio- 
phores are macronematous, acroauxic, and determinate; and the formation 
of conidia is holoblastic and integrated and both inner and outer walls of the 
conidiogenous cell contribute to the formation of the conidium on a pedicel 
in a blowing-out process. 

After the release of the conidia, the ampulla collapses characteristically 
in concertina-like folds about well-marked septa, especially obvious in 
B. squamosa (Walker 1925; Viennot-Bourgin 1953), B. globosa (Raabe 
1938; Webster and Jarvis 1951), and B. ficariarum (Hennebert and Groves 
1963). This characteristic collapse of the ampulla is also figured in Klebahn's 
(1930) drawing of his B. cinerea f. douglasii, which both he and Zederbauer 
(1906) regarded as close to, or identical with, B. cinerea. After abscission 
a flat, rounded scar is left on the conidiogenous cell from which new conid- 
iophores may proliferate. A slight frill is left on the conidium after its 
abscission. 



Numerical taxonomy 

The genus Botrytis has been subject to a numerical taxonomic study 
(Morgan 1971a, \91\b). Applying two biometrical methods to the B. cinerea 
complex and using 107 quantitatively expressed characters in 33 isolates, 
Morgan concluded that the taxon is a complex of races, identifiable mainly 
on cultural characters, but none of the races is sufficiently distinct to warrant 
a new taxon. This conclusion agrees with the general conclusions of Men- 
zinger (1966a, 19666), Hennebert (1971), and Vanev (1972) that cultural 
characters can be manipulated to some extent, and have little value in 
differentiating races in B. cinerea. However, in an analysis of 12 taxa, Morgan 
(19716) was able to recognize two forms of B. cinerea; Type A was 
characterized by gray colonies, abundant spore production, and sparse or no 
sclerotia, and Type B colonies were cream or white on arabinose, raffinose, 
or sorbose media, with sclerotial production favored at the expense of 
conidia. 

Of the 12 taxa, Morgan (19716) was able to distinguish B. hyacinthi 
from both B. narcissicola and B. tulipae, which Brierley (1931) had suggested 
were conspecific; and Morgan also distinguished B. allii (B. aclada), B. 
byssoidea, B. cinerea (types A and B), B. fabae, B. paeoniae, B. polyblastis, 
and B. squamosa. Though Morgan produced a key that differentiates B. 
anthopila from B. spermophila, the two species were sufficiently closely linked 
in the numerical taxonomy to suggest conspecificity. The relationships be- 
tween imperfect species were not altered by considering also characters of 
the relevant perfect stages. 

17 



Biochemical differentiation 

Lilly (1963) grouped a number of fungi by their ability to utilize sorbose; 
B. cinerea utilized it, whereas Sclerotinia (Whetzelinia) sclerotiorum did not. 
Maas and Powelson (1972) found that B. convoluta also could not readily 
utilize sorbose and they suggested on this basis that B. convoluta had a 
greater phylogenetic affinity with W. sclerotiorum than with B. cinerea. 
Similarly, Maas and Powelson contrasted the poor utilization of lactose by 
B. convoluta with lactose utilization by B. cinerea (Townsend 1957) and the 
uniqueness of B. convoluta in producing a firm rather than a soft rot of Iris 
rhizomes. 



Variability 

Menzinger (1966a, 19666) reviewed the taxonomy of Botrytis species 
and in 12 species and 2 isolates — one of the B. allii (B. aclada) type and 
one of the B. cinerea type — showed how cultural conditions could con- 
siderably modify taxonomic characters. Thus, for example, 7 species and 
1 isolate were induced to form multiseptate conidia. This condition in B. allii 
(B. aclada) must cast considerable doubt on the validity of B. septospora from 
onion described by El-Helaly, Elarosi, Assawah, and Kilani (1962). Men- 
zinger similarly considered the dimension and shape of conidia and the 
characters of mycelia and sclerotia to be of doubtful value in taxonomy 
because of variation between cultural conditions; he also found difficulty in 
reconciling characters of the species studied by him with their original 
diagnoses. 

Vanev (1972) also manipulated conidial size and form and colony 
characters by altering the temperature and culture medium and found mor- 
phological changes to be reversible. 



SEXUAL REPRODUCTION 

Until 1929, the sexual process in the Sclerotiniaceae had been obscure 
and the genetic connection between Botryotinia spp. and Botrytis spp. had 
not been demonstrated (Buchwald 1949). De Bary (1884) and Brierley 
(19186) had considered the microconidia as true spores with no sexual 
function, but Whetzel (1929) suggested their role as spermatia, as in the 
rusts. Drayton (1932, 1934) finally demonstrated this role in the sexual 
mechanism of Stromatinia gladioli of the family Sclerotiniaceae. He specu- 
lated that the gelatinous, water-soluble matrix of the microconidial sporodo- 
chia would permit the water- or animal-borne transport of microconidia to 
the receptive bodies on host debris and so achieve 'spermatization', the 
process leading to the formation of apothecia. 

As a result of Drayton's work, the sexual status of Botryotinia species 
was determined. Groves and Drayton (1939) obtained apothecia from 
isolates of Botrytis of the cinerea type by adding microconidia to sclerotia or 

18 



to sterilized soil placed over sclerotia, but they did not attempt to equate the 
apothecial state with Botryotinia fuckeliana because of the then uncertain 
identity of de Bary's Peziza fuckeliana. Groves and Loveland (1953) in- 
vestigated the situation again and found that single ascospore cultures are 
self-sterile and show the bipolar type of mating behavior of Stromatinia 
gladioli (Drayton 1934). Successful crosses were made between 9 single 
ascospore isolates from apple, potato, and celery in Canada, and also between 
these and 2 isolates of Botrytis cinerea from grapevine in Switzerland, the 
site of de Bary's original collection. In all cases, apothecia were morpholo- 
gically similar to de Bary's Peziza fuckeliana and single ascospores gave rise 
to typical fructifications of Botrytis cinerea. The connection between Botryo- 
tinia fuckeliana and Botrytis cinerea was thus established. Sidorova (1972), 
however, failed to obtain apothecia of Botryotinia fuckeliana from isolates 
collected in different parts of the USSR. 

Drayton (1937) obtained the perfect stage of Botrytis convoluta by 
spermatization; Buchwald (1953) and Webster (1954) that of B. globosa; 
Elliott (1964) that of B. porri; Bergquist and Lorbeer (1968, 1972) that of 
B. squamosa; Drayton and Groves (1952) that of Botrytis narcissicola 
(designated Stromatinia narcissi); and Hennebert and Groves (1963) those of 
B. ranunculi and B. ficariarum. According to Hennebert (unpublished), 
B. globosa and B. porri are homothallic, B. ranunculi is hermaphroditic and 
self-fertile, and B. ficariarum is probably heterothallic. 

Bergquist and Lorbeer (1972) showed that compatibility in B. squamosa 
is controlled by a single locus with two alleles. Wild types were hermaphro- 
ditic, self-sterile, and cross-fertile, and interspecific crosses between B. squa- 
mosa and B. fuckeliana were unsuccessful. 

Apothecial and ascus formation in Botryotinia fuckeliana was described 
by Kharbush (1927). In the young hymenium, somewhat elongated binucleate 
cells arise from the anastomosis of the tips of hyphae and are cut off by a 
wall. Each of the two nuclei of each cell of this ascogenous hypha has a 
distinct membrane, nucleolus, and chromatin; at this stage, the cell elongates 
among the paraphyses and swells. When the young ascus has attained the 
length of the paraphyses, the nuclei fuse and almost immediately meiosis 
begins; Kharbush saw 2 chromosomes at each pole in anaphase. According to 
Kharbush two mitotic divisions then result in 8 nuclei, around which the 
cytoplasm is differentiated into biguttulate ascospores. The nucleus of each 
ascospore usually undergoes further division and the spores are thus binu- 
cleate. Istvanffi (1905) found ascospores to be usually 1 -nucleate, however, 
and only occasional large spores were 2- or 3-nucleate. 

Kharbush found no ascogenous hyphae such as occur in Stromatinia 
gladioli (Drayton 1934). The dicaryon phase is very brief and limited to the 
period of cell fusion as the asci are initiated. 

Microconidia in the Sclerotiniaceae are typically uninucleate, as are the 
terminal and subterminal cells of the phialide (Berthet 1964). 

Cytology in the Discomycetes was reviewed by Bellemere (1969). 

19 



PART 3 FORM AND FUNCTION 



ANATOMY AND MORPHOLOGY 



Mycelium 

The morphology and anatomy of the thallus of Botrytis spp., described 
by Istvanffi (1905) and Beaverie and Guilliermond (1903), are undistin- 
guished and typical of the Ascomycetes. Some caution is required in reading 
the second paper as it includes one sterile form, known as 'toile', which was 
later shown to have probably been a species of Rhizoctonia (Corticum vagum 
var. ambiguum) (Baldacci 1937; Baldacci and Cabrini 1939). Anastomoses 
between hyphae have often been noted and their significance is discussed in 
"Cytology" in PART 3. 

The pattern of hyphal growth and branching, regular for the Ascomy- 
cetes, was described by Smith (1924). Extension occurs at the hyphal apex 
and, from spore germination, the growth rate increases with time until a 
constant rate is reached. Branches arise some distance behind the apex. As in 
other septate fungi, aggregations of vesicles, "spitzenkorper", occur just 
behind the hyphal apex in B. cinerea (McClure, Park, and Robinson 1968). 
These bodies appear to be formed posteriorly and migrate to the apex of the 
hypha, where they fuse with the plasma membrane and liberate their contents 
as part of the growth process of the cell wall. They are stained with cationic 
dyes such as methyl green. 

'Microbodies' in hyphae of B. cinerea were described by Maxwell, 
Maxwell, Hoch, and Armentrout (1973). Septa are frequent and are per- 
forated by a simple pore. Intrahyphal hyphae may be seen frequently tra- 
versing old, empty hyphal cells (Istvanffi 1905) through this pore; the intra- 
hyphal hyphae may bear microconidiophores (Brierley 1918). 

In culture on defined media, the thallus of some species of Botrytis is 
sufficiently distinct to be of assistance in identification (Hennebert 1971): 
Botrytis anthophila and Botryotinia spermophila usually produce a slow- 
growing, immersed, and arborescent mycelium; B. porri has a gray radiate 
mycelium; B. calthae has a brownish prostrate colony; B. ficariarum has a 
creamy-white colony. Because all species can be induced to sporulate by 
manipulating the cultural conditions, taxonomy, even of the so-called sterile 
forms, does not depend on mycelial characters. 



Conidiophores and conidia 

The conidiophores of all species of Botrytis, except B. spermophila and 
B. anthophila, are tall, stout, dark-colored, and irregularly or dichotomously 

20 



branched. The conidiophores of some species — for example, Botryds cinerea 
and B. ficariarum — have a globose basal cell (Massenot 1958; Hennebert 
1973). Near the apex of each conidiophore are produced a number of short, 
dark, septate sporogenous branches, each with a terminal ampulla on which 
conidia develop synchronously on short, fine denticles. At intervals along the 
conidiophore, botryose clusters of conidia are often formed from short side 
branches that bear sporogenous cells, giving the appearance of nodal areas 
of sporulation. The conidia are hyaline or pigmented, ellipsoid-obovoid- 
globoid, usually continuous, and sometimes 1-3 septate (Ellis 1971; Henne- 
bert 1973). The conidia are smooth, although Massenot (1958) showed 
verrucose conidia in dry mounts of B. tulipae. Conidia germinate in nutrient 
solutions, but less readily in water, to form (usually) 1-5 germ tubes. 

Mason (1933, 1937) proposed the term radulaspores, originally for the 
spores borne directly on the ascospores of Nectria coryli, and appHed it to 
the synchronously produced conidia of B. cinerea. Because the radulaspores 
of A^. coryli are homologues of phialospores, the name cannot be applied to 
the conidia of B. cinerea (Hughes 1953). McCallan (1958) described the 
conidium of B. cinerea as a prolate spheroid and, in relation to fungicide 
studies, he calculated its volume from its dimensions (1 1.7 X 9.3 /^m; 6-15 X 
1-12 ixxn) to be 556 /xm^', with a density factor of 1.1. 

In all species, but conspicuously in B. squamosa and B. globosa 
(Walker 1925; Raabe 1938; and Webster and Jarvis 1951), the terminal 
branches of the conidiophore collapse in accordion-like folds on spore 
release. Klebahn (1930) portrayed this, without comment, in B. douglasii 
(B. cinerea). 

In the context of susceptibility to fungicides, Fisher and Richmond 
(1969), Fisher, Holloway, and Richmond (1972), and Richmond and Somers 
(1972) investigated the nature of the hydrophobic surface of conidia of 
Botrytis fabae. They found lipids on the surface with component fatty acids 
predominantly straight-chain, €230 and C23:], but surface hydrocarbons 
were almost entirely A?-alkanes, C20, C2i, and €22- Most species of Botrytis 
have hydrophobic conidia, although their surface structure has not been in- 
vestigated. 



Microconidia 

The hydrophilic microconidia, which occur in all species, are phialo- 
spores. Because they differ only slightly between species, they are of no taxo- 
nomic value. Phialides may occur on any part of the thallus, sometimes within 
old, empty hyphal cells, or directly from germinating macroconidia (Istvanfii 
1905; Beaverie and Guilliermond 1903; Brierley 1918^; Hino 1929; Drayton 
1932, 1937; Groves and Drayton 1939; Arnaud and Berthelet 1936; Berthet 
1964; and Sidorova 1972). Phialides are more usually formed, however, in 
what Whetzel (1945) termed spermodochia: fasciculate or tuberculate aggre- 
gations of branched spermatiophores, usually arising from single hyphal cells 

21 



and borne freely on the aerial mycelium. The spermodochia usually com- 
prise one or two series of globose metulae, bi- or tri-furcate; the terminal 
metula is somewhat shorter and more slender, bearing up to about 5 phialides 
(Hennebert and Groves 1963; Hennebert 1973). The phialides have collar- 
ettes (Brierley 1918^; Arnaud and Barthelet 1936; and Berthet 1964). The 
whole structure is white in mass and the globose microconidia (spermidia of 
Whetzel 1945; spermatia of Hennebert 1973) are hyaline, unicellular, 2-3 
/xm, and have a conspicuous lipid droplet. They are developed in chains and 
embedded in mucilage. 

Brierley (1918^) found that microconidial production was primarily a 
function of thallus age; relative humidity, light, temperature, and nutrition had 
little effect. 

De Bary (1884) and Brierley (19186) thought that microconidia 
functioned as true spores; indeed, Brierley claimed to have germinated them 
in water and in a nutrient broth to give a normal mycelium, although Istvanffi 
(1905) and Hino (1929) found them very difficult to germinate in vitro. Now, 
their sole function is believed to be one of spermatization; see "Sexual Re- 
production" in PART 2. 



Ch lamydospores 

Price (1911) and Brierley (19186) described chlamydospore-like bodies 
in cultures of Botrytis cinerea. They are thick-walled, larger than macroco- 
nidia (35-71 /xm, mostly 60-70 /xm in diameter) near the surface of the 
stroma, and are produced on separate hyphae that project from the surface 
of the sclerotium. They are usually terminal but sometimes intercalary. No 
germination was observed. Park (1954) obtained chlamydospores of B. 
cinerea in drops of distilled water and soil solutions when spore concentra- 
tions were high. They have a distinct double wall and dense contents. Rama- 
zanova (19586) described chlamydospores and gemmae as well as sclerotia 
in B. anthophila. 



Oidia 

Istvanffi (1905) and Brierley (19186) described globose oidia of B. 
cinerea formed by the fragmentation of hyphae in distilled water. These oidia 
were similar to the chlamydospores obtained by Park (1954). 



Haustoria 

Only in one host-parasite combination are haustoria known — that of 
the clover anther mold, B. anthophila (Silow 1933). 

22 



Appressoria 

Appressoria, essentially infection structures, are formed by the dichot- 
omous branching of germ tube and hyphal tips, apparently in response to 
a contact stimulus (Istvanffi 1905; Pfaff 1925; and Blackman and Welsford 
1916). Their function is more fully described in "Infection" in PART 4. 



Organs of attachment 

When, for example, a grape berry is attacked by a mycelium established 
in its neighbor, well-developed organs of attachment are formed between the 
two (Istvanffi 1905). Initially, the organs of attachment resemble sclerotial 
initials and appressoria, formed by dichotomous branching of hyphae, but 
later they develop as more or less parallel series of dichotomously branching 
hyphae, with 1 or more series of branches. Eventually they form a fairly 
massive structure 1-2 mm in length. The tips of the hyphae, pressing against 
the cuticle of the healthy berry, swell somewhat, like appressoria, and pene- 
tration occurs. 



Sclerotia 

All species of Botrytis form sclerotia firmly attached to the substratum 
and their morphology is of some assistance in taxonomy. Although sclerotia 
of Botryotinia porri are large, 10-40 mm in diameter, and those of Botrytis 
tulipae and B. galanthina are less than 1 mm, it is doubtful whether species 
can be confidently divided into Microsclerotiophorae and Macrosclerotio- 
phorae, with the dividing line at 2 mm, as proposed by Buchwald (1949). 
Sclerotia of Botryotinia convoluta are characteristically large and cerebriform, 
those of B. ficariarum are flat and clearly marginated, and those of B. calthae 
are brown and diffuse (Hennebert and Groves 1963). Sclerotia of the last two 
species are also anatomically distinct; those of B. calthae have a much more 
compact internal structure. 

In culture, some species produce their sclerotia in characteristic patterns: 
B. tulipae, B. hyacinthi, B. galanthina, and B. paeoniae have equidistant scle- 
rotia; B. porri produces sclerotia at the margin only. But because the arrange- 
ment of sclerotia can be manipulated to some extent by cultural conditions, 
this criterion is unsatisfactory. 

The structure of the sclerotium has been described several times (de 
Bary 1884; Beauverie and Guilliermond 1903; Istvanffi 1905; Reidemeister 
1909; Townsend 1952, 1957; Townsend and Willetts 1954; Hennebert and 
Groves 1963; Willetts 1969, 1972; and Nonaka and Kaku 1973). Hyphal tips 
branch repeatedly and dichotomously; the branches have many septa and 
may also fuse to form the characteristic structure, which is at first hyaline but 
later turns brown or black because of deposition of melanic pigments in the 
outer rind (Brierley 1920; Willetts 1969). 

23 



In Botrytis allii (B. aclada) the sclerotium has a rind 6-8 cells thick, 
rounded, and thick-walled; a narrow cortex 3-4 cells thick, thin-walled and 
pseudoparenchymatous, with dense contents of stored materials; and a large 
central medulla of filamentous hyphae loosely arranged in a gelatinous matrix. 
The sclerotium of B. cinerea is similar but with a thinner rind and a thicker 
cortex (Townsend and Willetts 1954). The outer surface of the sclerotium 
of B. cinerea is composed of closely arranged, thick-walled hyphae with 
outward-projecting tips, A film covering most of the surface appears to be 
an accumulation of dried pigment (Willetts 1969). 

Istvanffi (1905) distinguished 4 types of sclerotial development in B. 
cinerea: (i) from single sclerotial initials ('pelottes'); (ii) from a felted layer 
of closely packed, roughly parallel hyphae, beneath and raising the host 
cuticle; (iii) the same, containing a layer of pelottes; and (iv) from a layer 
of felted hyphae containing a random arrangement of pelottes. He also de- 
scribed small, conical pseudosclerotia in thickened hyphae, which later 
develop directly into conidiophores. Loosely arranged, thickened hyphae, 
lying beneath the cuticle in a single layer, comprised another resting structure. 
In the field, sclerotia germinate in one of three ways (Istvanffi 1905): (i) conid- 
iophores arising within the medulla push singly through the rind; (ii) conidio- 
phores arise in a tuft from a small stromatic cushion formed at the surface 
of the sclerotium; and (iii) after a resting period of 2-6 mo, the rind cracks 
open at any point to reveal the elongating stipe of an apothecium, and some- 
times 2-6 apothecia arise from one sclerotium. 

During germination, the sclerotial cells empty except those around the 
base of the conidiophores, or stipe; the hyphae collapse and the intercellular 
spaces become filled with air. 

The ability of sclerotia to produce apothecia decreases with time; after 
9-12 mo they are able to produce only sterile apothecia, but the conditions 
affecting whether or not sclerotia germinate, and how they germinate, have 
not been determined. In culture and after surface-sterilization, sclerotia give 
rise to vegetative mycelium. Sclerotia of B. tulipae were believed to germinate 
in this way in soil (Beaumont, Dillon Weston, and Wallace 1936), but Coley- 
Smith and laved (1972) observed this only in sclerotia very close to tulip 
bulbs. 

The most frequent mode of germination is conidiophore production. 
When mature, the sclerotia of B. cinerea can germinate over a wide range of 
temperatures (3-27 °C) to form a succession of conidiophores for as long as 
2 mo, and in the field they germinate mostly in the spring and autumn (Vanev 
1966; Kublitskaya and Ryabtseva 1970). At 5°C, after exposure to near- 
ultraviolet light, sclerotia of B. convoluta gave rise to up to 6 crops of conid- 
iophores until 75% of their original dry weight was expended (Jackson and 
Patrick 1969; Jackson 1972). Resporulation was dependent on re-exposure 
to ultraviolet light at 25 °C but not at 5°C and it was suppressed by the 
continued presence of old conidia but not by that of old conidiophores alone. 
Sclerotia of B. fabae also give several crops of conidia (Yu 1945), but those 
of B. tulipae decay soon after the production of conidiophores in the winter 
and early spring (Coley-Smith and Javed 1972). 

24 



Some sclerotia of B. cinerea, however, do not give rise to conidiophores 
but in late summer germinate to form apothecia, which are viable for 20-30 
days at 3°C, but only for 3 days at 23°C (Istvanffi 1905; Kublitskaya and 
Ryabtseva 1970). 



Apothecia 

During apothecial formation in Botryotinia fuckeliana, the generative 
hyphae grow through the cortex of the sclerotium (Istvanffi 1905; Kharbush 
1927). A columnar structure, the stipe, forms and when it is about 4-5 mm 
long a hard cap develops, which differentiates into the apothecial disc. Some- 
times the base of the stipe is invested in rhizoidal hyphae (Hennebert and 
Groves 1963). The apothecium is cupulate, stalked, and usually some shade 
of brown; the cup is infundibuliform to discoid and sometimes has a reflexed 
margin in age. 

The anatomy of the apothecium has been described several times (see 
PART 2, "Taxonomy"), particularly well in the case of Botryotinia calthae, 
B. ficariarium, and B. ranunculi (Hennebert and Groves 1963). The apothe- 
cium comprises (Korf 1958, 1973) the hymenium, a palisade layer of asci 
with paraphyses of about the same length as asci; the hypothecium (sub- 
hymenium of some authors), a tightly arranged mass of hyphae below the 
hymenium; and the excipulum, which envelops the hypothecium and the 
margin of the hymenium. The excipulum is divided into two parts: the ectal 
excipulum forms the outer layers of the tissue, including the margin of the 
apothecium; and the medullary excipulum forms the layer between the ectal 
excipulum and the hypothecium. The terminology of the various tissue types 
is defined by Korf (1958, 1973). 

The asci are unitunicate, inoperculate, and long clavate; the tip of each 
ascus is thickened with an apical pore-plug giving a positive blue reaction 
with iodine (J + ). 

The ascospores, 8 per ascus, are uniseriate, hyaline, unicellular, smooth, 
and obovoid-ellipsoid, sometimes asymetrically so (Istvanffi 1905). Some- 
times more than 8 spores may be in the ascus and they may germinate there 
(Hennebert and Groves 1963). The paraphyses may be branched and, at the 
tip, clavate. 

In a medium such as grape juice, the ascospores may germinate directly 
to form a conidiophore of the Botrytis type (Istvanffi 1905), but usually a 
mycelium is formed and eventually sclerotia and conidiophores (Kharbush 
1927). 



Ultrastructure 

The ultrastructure of conidia of Botrytis cinerea, which was examined 
by Hawker and Hendy (1963), Buckley, Sjaholm, and Sommer (1965, 1966), 

25 



and Gull and Trinci (1971), seems similar to that of many other fungi. 
Dormant conidia of Botrytis cinerea have a 2-layered wall: a thin electron- 
dense outer layer and a thicker inner layer. The cytoplasm is typically multi- 
nucleate and contains numerous rodlike mitochondria. Short strands of endo- 
plasmic reticulum appear to originate from the cytoplasmic membrane lining 
the cell wall; they are continuous with the mitochondrial and nuclear mem- 
branes and storage bodies, which suggests that they are involved in organelle 
development. At germination, some of the mitochondria appear cup-shaped 
and lobed; the strands of endoplasmic reticulum are much longer, more 
numerous, and often close to nuclei. The nuclei appear to divide early in 
germination. When the conidium germinates, 3 new layers appear between 
the original wall and the cytoplasm. The inner two of these are continuous 
round the cytoplasm; the third is formed only near the point of germ tube 
emergence and is continuous with the germ tube wall. The original wall 
thickness would be expected to decrease as it stretches during spore swelling 
at germination, but the formation of new layers increases wall thickness from 
about 260 nm to 340 nm. 

The outer cell wall ruptures as the germ tube emerges. The contents of 
the conidium, leaving behind large vacuoles, flow into the germ tube, whose 
wall is elastic and invested by a mucilaginous sheath. An apical corpuscle 
appears in the germ tube and a cross wall is laid down near the base. 

The wall of the dormant conidium of B. fabae is unornamented and 
consists of microfibrils in a granular matrix in 2 distinct but similar layers; 
branched invaginations of the plasmalemma are a distinctive feature (Rich- 
mond and Pring 1971a). On germination, the ramifications are reduced as the 
conidia swell and they disappear after the germ tube is formed. Three different 
types of particles are present on the inner surface of the plasmalemma and 
the mitochondria have dense spherical inclusions, not previously known in 
fungi, which disappear when germination begins, as do glycogen particles. 

The endoplasmic reticulum, which appears as short strands associated 
with the cell wall in the dormant conidium, increases on germination and 
multiple strands surround the nuclei. Vesicles pass through the plasmalemma 
to form simple vesicular lomasomes and, by a similar process, complex tubular 
lomasomes form in young hyphae. Prevacuoles become vacuoles and an apical 
corpuscle appears in the germ tube. No Golgi apparatus is known. The fungi- 
cide benomyl interferes with ultrastructure and development of the cell wall 
in B. fabae (Richmond and Pring 1971/?); the germ tube is swollen and 
distorted and much branched. 

The structure of the hyphal wall of Botrytis narcissicola was investigated 
by Jones, Farmer, Bacon, and Wilson (1972). X-ray powder data indicated 
the presence of chitin and the infrared spectrum indicated that of /?-(l-3) 
glucan; hydroly sates included glucose and mannose. A glucan constituent, 
sclerotan, was found in B. cinerea and B. tulipae as well as in B. narcissicola. 
Electron microscopy showed microfibrils on the inner surface of the hyphal 
wall and on the septum, which is perforated by a central pore bounded by a 
thick rim. 

26 



The ultrastructure of hyphae of B. fabae invading tissues of Vicia faba 
and the ultrastructure of the invaded tissue were described by Abu-Zinada, 
Cobb, and Boulter (1973). Growth of the fungus was restricted (see PART 4, 
"Quiescent Infections"). The only difference between hyphae outside and 
inside the host was the somewhat less dense cytoplasm of the invading hyphae. 
Numerous lomasome-like structures were formed at the junction between the 
fungus and host; Abu-Zinada et al. suggested that these might be the sites 
of hydrolytic, cell-wall-disrupting enzymes. Incubating the fungal mycelium 
in an extract of infected leaves resulted in considerable disorganiAtion of 
fungal ultrastructure; thus these enzymes perhaps form the basis of the lesion- 
restricting mechanism. 



CYTOLOGY 

The vegetative cells and asexual conidia of Botrytis species may be 
heterokaryotic, and the hyphal cells, with a few exceptions, are multinucleate 
(Menzinger 1965, 1966«, 1966/?). As many as 120 nuclei per cell have been 
recorded in an isolate of B. cinerea, whereas uninucleate hyphal cells were 
found in B. allii (B. aclada), B. cinerea, B. convoluta, and B. narcissicola. 
Between these extremes, Menzinger (1965) found an average of 2 to nearly 
50 nuclei in hyphal cells and up to 20 nuclei in single-celled and multi-celled 
conidia, although there was no correlation between the number of nuclei per 
cell and conidium size. Welsford (1916) had earlier noted the tendency of 
nuclei in rapidly growing hyphae of B. cinerea to be associated in pairs, 
termed conjugate nuclei. The tendency was less obvious in hyphae growing in 
water and in Vicia faba leaves, and Welsford thought that nuclear divisions 
in well-nourished hyphae were so rapid that the nuclei did not have time to 
separate widely before undergoing mitosis again. Menzinger (1965) found 
nuclei of all shapes, the shape apparently depending on the rate of cell growth. 

Menzinger (1965) found that the number of nuclei varied from cell to 
cell in the same th alius; nuclei were most numerous in the sporogenous 
ampullae and terminal cells of the hyphae, but markedly less numerous in 
subterminal cells. The heterokaryotic condition was maintained by the transfer 
of nuclei across hyphal anastomoses, just as Kohler (1930) and Hansen and 
Smith (1932, 1935) had found, and Menzinger also observed the passage of 
nuclei from cell to cell through the septal pore. 

Heterokaryosis was intensively studied by Hansen and Smith (1932«, 
1932^, 1934, 1935) and Hansen (1938) as a source of variability in Botrytis 
spp. Kohler (1930) had earlier observed contact between hyphae of B. allii 
(B. aclada) and B. narcissicola, but it is doubtful that transfer of nuclei 
occurred. Hansen and Smith (1932a, 1932^) obtained 47 isolates of the 
B. cinerea type, from each of which subcuhures were repeatedly made by 
single-conidium transfers. After many such transfers, there was a wide range 
of morphologically distinct strains in culture. Some strains remained similar 

27 



to the parent strain throughout subculturing and were termed homotypes. 
Other strains continued to produce homotypes and further inconstant hetero- 
types. Anastomoses were common; hyphal cells and conidia were multi- 
nucleate, the number of nuclei ranging from 6 to 1 8 per cell in one homotype 
and from 3 to 9 in another. Hansen and Smith (1932^) considered that such 
cells could act as heterokaryotic propagules. 



Hansen and Smith (1934, 1935) also noted occasional anastomoses in 
co-culture between the hyphae of two distinct species, B. allii (B. aclada) and 
B. ricini. The fungi were first passed through several subcultures to obtain 
uniformity and then spores from them were mixed to give 20 co-cultures: 
6 B. allii type, 9 B. ricini type, and 5 different types, intermediate between 
B. allii and B. ricini, though more resembling B. ricini. From 1 of these 
5 intermediate types, 20 subcultures were made, all of which were unlike 
B. allii and B. ricini. Hansen and Smith considered that they had established 
new homogenic forms that were stable and distinct enough to be regarded 
as new varieties or even as new species. They suggested that the production 
of aberrant homotypes resulted from gene changes in B. ricini brought 
about by the association of nuclei of B. allii in interspecific anastomoses, 
rather than from the combination of homogenic nuclei. 



Hansen (1938) applied similar methods to an analysis of the dual phe- 
nomenon in B. cinerea, the condition in which the fungus is made up of 
2 culturally different elements. He showed that a strain, stable in producing 
mainly mycelium in culture, mixed with a stable, predominantly sporing cul- 
ture, formed cultures of intermediate character. The cultures formed varied 
in appearance from almost the mycelial type to almost the sporing type, and 
subcultures gave mycelial, sporing, and again intermediate types. Of 309 
isolates of B. cinerea, 144 showed this dual phenomenon, which Hansen 
regarded as the normal condition. He regarded certain reactions, such as 
sectoring, reversion, and loss of ability to sporulate, as resulting from a 
change to the homotype condition. 



Menzinger (1966/?), also using single-conidium cultures of several species 
of Botrytis, confirmed the results of Hansen and Smith (1934, 1935) in their 
studies of co-cultures and showed that anastomoses often occurred between 
species and between isolates of the same species. However, only once was a 
morphologically distinct and stable intermediate type obtained; it was from a 
co-culture of two isolates of B. cinerea from Gloxinia. 



Lauber (1.971) obtained a number of strains from single-conidium selec- 
tions of B. cinerea over six subcultures; they were differentiated by several 
physiological characters such as growth on nutrient agars and in soil, toler- 
ance for actidione, and production of citric acid. He concluded that his 
original five wild isolates were genetically heterogeneous and heterokaryotic. 

28 



VARIANTS 



It has long been recognized that Botrytis spp. in culture can be divided 
into 3 types — mycelial, sporulating, and sclerotial — although the division 
is often not clear. This division has led to considerable taxonomic confusion 
(Killian 1926) because later work has demonstrated the fallibility of using 
cultural characteristics as taxonomic criteria. 

Only one case is known of a clearly distinct morphological race: an 
isolate of B. cinerea from Crassula perforata, apparently lacking a phenolic 
oxidase system, had white sclerotia, but was otherwise of typical form and 
equally as pathogenic as normal black-sclerotial isolates (Brierley 1920). 

Most other workers have found morphological characters in culture to 
vary with environmental and nutritional conditions; for example, Vanev 
(1972) and Shidla (1912a, 1912b) found that conidia in B. cinerea, B. 
paeoniae, B. tulipae, and B. gladiolorum differed in size between a given host 
and culture, and differed again in size when re-isolated from artificially 
infected hosts. Some other workers, perhaps because they worked with rela- 
tively few isolates, have persisted in recognizing distinct morphological races. 
Thus, Berkeley (1924) found 4 morphologically distinct races of B. cinerea 
isolated respectively from geranium, squash, sunflower, and hemp; and 
Jorgensen and Weber (1929) found another on raspberry, which did not 
sporulate in culture. Abdel-Salem (1934) isolated 2 forms of B. cinerea from 
lettuce, which formed in culture predominantly either sclerotia or conidia. 
Those that formed conidia could be further divided on the basis of conidial 
shape and size: type A conidia were obovoid-oblong, measuring 11.1 X 7.25 
jam and type B were more round, 9.7 X 8.0 /xm. Similarly, Gupta (1960) 
found morphological, cultural, and physiological differences between isolates 
from Dolichos lablab and Tagetes patula; conidia from D. lablab were numer- 
ous, subglobose, and 7-10 X 6-9 ^m and the sclerotia were large, hard, 
and black, whereas the conidia from T. patula measured 9-12 X 7-9 ^am 
and the sclerotia were smaller, soft, and dark gray. Gupta also found physio- 
logical differences, principally in their production of pectinases. Nyeste (1960) 
found similar differences in polygalacturonase activity among isolates of B, 
cinerea. 

Another form, apparently of B. cinerea, occurred on kenaf. Hibiscus 
cannabinus, in Peru and Florida (Perez and Summers 1963). This form was 
considered to differ from B. cinerea and B. hortensis previously reported on 
H. esculentus. 

Saponaro (1953) concluded that isolates of B. cinerea from grapevine 
in different parts of Italy could be divided by conidial size in vitro into 7 
morphological races; Pesante (1947), Kublitskaya and Ryabtseva (1969), 
Kublitskaya and Rubitskaya (1969), and Gorlenko and Manturovskaya (1971) 
came to a similar conclusion. Courtillot, Lamarque, Juffin, and Rapilly (1973) 
also found differences in the morphology of conidia, microconidia, and scle- 

29 



rotia, and in conidial germination and temperature relations among isolates 
of B. cinerea from different regions of France. 

Nonaka and Morita (1967) recognized 8 sclerotial types among 80 iso- 
lates of B. cinerea from 56 host species, but 80% of them changed their 
type with temperature. The isolates had different temperature optima for 
growth; 79% of them grew best at 20°C, 6% at 15°C, and 15% at 25°C; 
most sporulated best at 10°C, and all were pathogenic to azalea petals and 
broad-bean leaves. 

Heald and Sprague (1926), Morquer (1933), and Peyronel (1934) ob- 
tained isolates of B. cinerea that consistently produced a red pigment in agar. 

Variability in Botrytis anthophila was noted by Ramazanova (1958fl); 
isolates from 5 regions of the USSR showed morphological, cultural, and 
pathogenic differences. An isolate from Leningrad area was the most patho- 
genic to clover, and one from Bashkir the least. A variant that grew well on a 
potassium-deficient medium was more pathogenic than the isolate from which 
it was originally derived, and, moreover, retained its cultural characters on 
reisolation. Buderacka-Niechwiejczyk (1970) also recognized different forms 
of B. anthophila in culture. 

When more isolates are studied or when cultural conditions are varied, 
it becomes evident that morphological forms are less easily distinguished. For 
example, Paul (1929) found that sclerotial formation by B. cinerea in culture 
was encouraged by lowering the temperature of incubation to 12°C, and by 
incubating in the dark or in high relative humidity. In richer media, sclerotial 
formation in the dark tended to occur at the edge of the petri dish, but 
because darkness was achieved by wrapping dishes in black paper, the effects 
of impeded gas and water vapor exchange cannot be excluded. On the other 
hand, sporulation was encouraged in illuminated cultures, at a temperature 
of 27 °C, and at lower relative humidities. Despite being able to manipulate 
morphological characters in this way, Paul nevertheless recognized 3 types: 
mycelial, sclerotial, and sporulating. There were no distinct differences in 
conidial size among these types, but the sporulating races were generally 
slower-growing. The mycelial isolates were the most actively parasitic, as is 
to be expected if considered in the light of inoculum potential (q.v.), and 
the sclerotial isolates the least pathogenic. All types achieved the penetration 
of formalized gelatine membranes equally well, and Paul was unable to 
attribute differences in pathogenicity to differences in pectinase production. 

Marked and consistent differences in pathogenicity between isolates of 
B. cinerea on stored cabbage were obtained by Yoder and Whalen (1973). 
Eleven isolates could be divided into 5 groups differing significantly in the 
rate at which they degraded wounded and unwounded tissue. 

Barnes (1930, 1931) induced variation in B. cinerea by exposing conidia 
to sublethal heat before sowing on agar. Of 520 cultures from treated conidia, 
424 failed to germinate, 20 grew indistinguishably from the check, 64 showed 
shght variation in growth, and 12 showed marked morphological variation. 

30 



Of the 12 with marked morphological variation, 4 were stable over 2 years: 
1 produced many sclerotia and few conidia, 2 formed white myceUal colonies, 
and 1 was characterized by the production of microconidia that germinated 
readily; one subculture of the last variant produced some white sclerotia 
(cf Brierley 1920). The remaining 8 of the morphological variants slowly 
reverted to original type, including one with pink sclerotia, which perhaps 
represented an incomplete state in melanin pigmentation. 

Owen, Walker, and Stahmann (1950) investigated the variability in 
onion neck-rot fungi. Wild-type isolates of Botrytis allii (B. aclada) and of 
B. byssoidea, sometimes suspected of being conspecific, caused similar symp- 
toms, although B. allii sporulated more profusely. An atypical isolate of 
B. allii, obtained once from the wild, was induced to form morphologically 
distinct types in culture by treatment with the mutagen vatihyX-bis (|8-chlo- 
roethyl) amine, but none resembled B. byssoidea. Similarly, wild-type forms 
of B. allii were induced to form mycelial types, but they soon reverted to 
the original type on subculturing. Owen et al. considered that they had 
failed to demonstrate that B. allii and B. byssoidea were conspecific, and con- 
cluded that these fungi, often confused on onion, were indeed separate species. 

Bergquist and Lorbeer (1973) induced morphological mutants in Botryo- 
tinia squamosa by treating ascospores with N-methyl-N-nitro-N-nitrosoguani- 
dine. Each form apparently carried several mutant genes that controlled 
production and pigmentation of sclerotia, formation of appressorial fans, com- 
pactness of colony growth, growth rate, sporulation, and tolerance for 
dichloran. 

Lauber (1971), starting with five wild-type isolates, obtained a number 
of physiologically distinct lines and showed that conidial size, although closely 
related to the number of nuclei per conidium, also depended on the age of 
the culture, pH, C:N ratios and amounts in the medium, and relative humidity. 
He thus substantiated Menzinger's (1966^, \966b) conclusions. 



Adaptation to fungicides 

Of profound importance in plant pathology is the special case of forma- 
tion of physiologic races of Botrytis spp. adapted to fungicides. 

Roy (1947) and Reavill (1950, 1954) were apparently the first to note 
that Botrytis cinerea could tolerate the presence of the chlorinated nitroben- 
zene group of fungicides in the vapor phase and could produce resistant 
strains in culture in their presence. Fungistasis, rather than fungicidal activity 
by these materials, was also demonstrated by Brook and Chesters (1957). 
Priest and Wood (1961) further investigated tolerance and the induction of 
resistant strains in B. allii growing in the presence of the vapor phase of some 
chlorinated nitrobenzenes. At first growth was very slow, the hyphae were 
distorted, and sporulation was reduced or suppressed, but eventually more 
rapidly growing strains appeared that more resembled the original strain and 

31 



that had apparently normal hyphae. The most resistant strain was that in- 
duced by 2,3,4,6-TCNB, followed in effectiveness by 2,3,5,6-TCNB, 2,3,4,5- 
TCNB, and PCNB. The strains resistant to TCNB and PCNB were also 
resistant in some degree to diiodo, dibromo, and dichloronitrobenzenes, to 
benzene, to 2,3,5,6-tetrachlonitroaniline, and to 2,6-dichloro-4-nitroaniline 
(dichloran). Resistant strains retained their resistance throughout subculturing 
for at least 18 mo and were as pathogenic to onion as the original strain. 

Esuroso, Price, and Wood (1968, 1971) further investigated the effect of 
cultural conditions on the germination of conidia of B. cinerea in the pres- 
ence of PCNB (quintozene), TCNB (tecnazene), and dichloran; and they 
analyzed the conidial population in resistant strains. About half the spores 
formed by resistant strains growing in the absence of fungicide produced 
resistant colonies when re-exposed to them, whereas all the viable spores of 
the same strains continuing to grow in the presence of the fungicide produced 
resistant colonies, although some of the spores failed to germinate. 

The growth of dichloran-tolerant strains of B. cinerea was unaffected 
by dichloran at 2 g/litre in liquid media (Lankow 1971), and on solid media 
their growth was stimulated 60% by 0.1 g/litre and normal germ tubes were 
formed. Susceptible strains were inhibited by concentrations greater than 
5 X 10~5 M; conidia germinated but the germ tubes disintegrated. Crystals 
appeared in hyphal tips and growth ceased within 5-10 min of exposure. 

Parry and Wood (1958, 1959fl, 1959^) demonstrated the ability of coni- 
dia of B. cinerea to germinate on agar media containing 300 ppm copper as 
sulfate, 0.375 ppm phenylmercuric acetate, 31 ppm thiram and similar con- 
centrations of zineb, ziram, and nabam, 125 ppm ferbam (and up to 
500 ppm in one case), and 250 ppm captan. The volume, and hence depth 
of agar in petri dishes, was critical in the initial stages of the adaptation 
process and spores germinated mainly at the edge of the agar. By taking 
successive subculture inocula from the edge of colonies the tolerated level of 
the fungicides was increased, for example, to 250,000 ppm captan and to 
12 ppm phenylmercuric acetate, and the tolerance was maintained through 
several subcultures in the absence of the fungicide. The ability of these strains 
to survive selection pressures in the field was not tested. 

Golyshin and Abelentsev (1973) noted synergistic effects in the adapta- 
tion of B. cinerea to zineb, zinc salicylanilide, and their mixture. 

Kovacs and Garavini (1959) found that not only did B. cinerea tolerate 
the presence of some organic fungicides, but some, for example, captan and 
thiram, when in low concentration in agar, stimulated germination of conidia. 

A race of B. cinerea, tolerant of the systemic fungicide benomyl, was 
isolated by Bollen and Scholten (1971) from Cyclamen sprayed 2 wk pre- 
viously with 0.0625% benomyl, a rather high rate of application. Growth 
of this race was inhibited in vitro by benomyl at 1000 ^ag/ml; another isolate 
from unsprayed Cyclamen was inhibited at 0.5 ixg/m\. The benomyl-tolerant 
isolate was also tolerant of methyl thiophanate, furidazol, and to a lesser 

32 



extent, thiabendazole. Its tolerance for benomyl was retained through 20 
weeks of repeated subculturing in the absence of benomyl. 

Bollen and Scholten (i971) and Dommelen and Bollen (1973) consid- 
ered that the exceptional pathogenicity of the tolerant race on Cyclamen 
might also result in part from the inhibition of benomyl-sensitive antagonists. 
The tolerant strain grew rather slowly, and Bollen and Scholten questioned 
its ability to survive in the wild in the absence of benomyl, though this was 
not tested. Jarvis and Hargreaves (1973), however, isolated a strain of B. 
cinerea tolerant of 1000 ppm benomyl that had been applied to strawberry 
plants a year previously and also found a tolerant strain on raspberries some 
50 m from a benomyl-treated crop. Ehrenhardt, Eichhorn, and Thate (1973) 
showed that the natural population of spores of B. cinerea in a vineyard had 
a wide range of tolerance for benomyl and they considered that continued 
exposure of the population to this and related materials would increase the 
proportion of tolerant isolates. Watson and Koons (1973) and Miller and 
Fletcher (1974) made similar observations on B. cinerea in greenhouse crops, 
and Jordan and Richmond (1974) in strawberries. 

In general, benomyl-tolerant isolates of B. cinerea are susceptible to 
normal field concentrations of other unrelated fungicides (Jarvis, unpub- 
lished), but Jarvis and Slingsby (unpublished) obtained one from Rosa in 
Canada that was somewhat tolerant of captan, copper, ferbam, dyrene, and 
chlorothalonil, but not of dichloran or Dikar. 



GROWTH 



Effects of temperature 



The effect of temperature on germinating conidia of Botrytis cinerea 
has been determined by a number of workers including Schneider-Orelli 
(1912) and Brooks and Cooley (1917) who recorded germination at 0°C on 
corn meal agar within 31 days, Doran (1922) who found a maximum tem- 
perature for germination of 26°C and a minimum temperature of 7°C, Brown 
(1922c) who obtained good germination at 5°C, and Hawker (1950) and Haas 
and Wennemuth (1962) who germinated spores between 1°C and 10°C (80% 
in 40 days and 95% in 14 days at the respective temperatures). 

Brooks and Cooley (1917), Brown (1922c), Schneider-Orelli (1912), and 
Adair (1971), among many others, have data on the effect of temperature on 
mycelial growth in B. cinerea. The mycelium is able to grow at low tempera- 
tures; Schneider-Orelli (1912) recorded appreciable growth at 0°C on nutrient 
gelatine in 35 days. The growth rate is optimum at about 20-22 °C and de- 
creases markedly above 25 °C. Similar results were obtained for B. squamosa 
by Stinson, Gage, and MacNaughton (1958) and Shoemaker and Lorbeer 

33 



(1971). Shiraishi, Fukutomi, and Akai (1970^) found a somewhat higher 
optimum temperature, 24-28°C, for mycelial growth of B. cinerea on potato 
sucrose agar, with a minimum of 0°C and a maximum of 35 °C. 

Hennebert and Gilles (1958) distinguished 2 optimum temperatures in 
early growth of B. cinerea. Spore germination, lasting about 5 h, had an 
optimum of 20°C, but after about 18 h, germ tube growth became dependent 
on external nutrients and the optimum temperature was then 30 °C. 

After growth of B. cinerea at the optimum temperature of 22 °C to the 
point of incipient sporulation, Jarvis (unpublished) transferred cultures to 
other temperatures. The optimum temperature for sporulation from this point 
was 15°C; sporulation fell rapidly at higher and lower temperatures in con- 
trast with the mycelial growth rate and was very slow at both 10°C and 
24 °C. Brooks and Cooley (1917) found that sporulation occurred at 5°C and 
10°C within 10 to 31 days of inoculation of agar plates. 

From field work, Jarvis (19626) deduced that sporulation in a raspberry 
plantation did not occur to any appreciable extent at temperatures below 
about 12°C but could occur overnight in suitable conditions. 

Shiraishi, Fukutomi, and Akai (1970a) studied synchronous conidial 
formation in cultures of B. cinerea at 24 °C on potato sucrose agar and on a 
sponge matrix. Formation occurred about 3 days after inoculation of potato 
sucrose agar and within 24 h after transfer of a shake-culture inoculum to 
the sponge matrix. 

The effects of temperature on sporulation of B. tulipae were defined by 
Yamada, Kajiwara, and Ozoe (1972). 

Temperatures favoring mycelial production in fi.cmerea generally depress 
sclerotial production and vice versa (Townsend 1952; Vanev 1966; and 
Kublitskaya and Ryabtseva 1972). Morotchkovski and Vitas (1939) gave 
11-1 3 °C as the optimum temperature range for sclerotial production in B. 
cinerea but 12-22°C for sporulation and 27-28 °C for appressorium forma- 
tion. Kochenko (1972) gave data on sclerotia; they germinated at tempera- 
tures above 2°C and the optimum temperature for germination was between 
22°C and 24°C. 



Effects of relative humidity 

There have been many studies on the effect of relative humidity on the 
germination of fungal spores. The results, however, must be viewed with 
extreme caution, especially in atmospheres of relative humidities greater than 
90%, because the usual limits of control in this type of experiment can easily 
permit the temperature to fall below the dew point, so that spores come to 
lie in condensate (Schein 1964). 

Thus, Rippel (19306) found 100% germination of conidia of B. cinerea 
and a Botrytis sp. at 20°C, 15°C, and 5°C in 100% RH when, almost cer- 

34 



tainly, the conidia must have been lying in condensate. There was complete 
germination of the Botrytis sp. at 95% RH, 80-85% germination at 90% 
RH, and none at 85% RH. At 95% RH, 80% of conidia of B. cinerea 
germinated at 15°C and 5°C and all germinated at 20°C; at 90% RH, 85% 
of conidia germinated at 20 °C, and none at lower temperatures or lower 
humidities. Similarly, Ilieva (1970) claimed germination of conidia of B. 
cinerea in the absence of free water. 

Snow (1949) concluded that conidia of B. cinerea require high levels of 
moisture for germination (93-100% RH) and Sirry (1957«) found that at 
21 °C, conidia of B. allii (B. aclada), B. cinerea, B. fabae, B. tulipae, and 
B. squamosa germinated at 100% RH, but not at 95% RH. 

Yarwood (1950) found that the water content of conidia of B. cinerea 
was only 17% of their fresh weight but that a high proportion was 'hygro- 
scopic water' when the conidia were on glass and in equilibrium with the 
laboratory air (42-51% RH). He thought that the hygroscopic water was 
probably much less active physiologically than the non-hygroscopic (total less 
hygroscopic) water. Imbibition of water is probably a prerequisite for germina- 
tion; soon after their immersion in water, conidia of B. cinerea swell slightly, 
reaching a maximum in about 3 h (Ekundayo 1965). P is interesting to note 
that Snow (1949) found a lag period before conidia of 3. cinerea (from cul- 
tures 1-2 mo old) germinated if they were applied dry to dry gelatine, and 
then equilibrated in atmospheres of different RH. At 100% RH, the lag 
was 1 day; at 95% and 93% RH 2 days, and at lower humidities germination 
did not occur. The lag phase may be interpreted as a period during which 
sufficient water is being imbibed from the atmosphere, or more likely from 
condensate. 

Most species of Botrytis seem to sporulate best in less than saturated 
atmospheres; then, the conidiophores are short and bear numerous spores 
that are readily dispersed (Paul 1929; Hawker 1950). In a saturated atmo- 
sphere, however, the conidiophores are long, of indeterminate growth, and 
bear few conidia. Hopkins' (1921) method for inducing sporulation in B. 
tulipae in petri dishes, by partially uncovering cultures overnight to promote 
drying, seems applicable to all species. 

Apothecia are usually produced in conditions that are cool and moist, 
but otherwise undefined (for example in Botryotina convoluta, Drayton 1937 
and in B. fuckeliana, Kochenko 1972); certainly apothecia dry out rapidly 
in dry atmospheres and presumably stop discharging spores, as they do in 
Whetzelinia sclerotiorum (Jarvis, unpublished). 



Effects of light 

Light has different effects on various growth processes according to its 
wavelength and plane of polarization, although all species are able to germi- 
nate and grow in the dark (Reidemeister 1909; Doran 1922). 

35 



A snow mold, a Botrytis of the cinerea type (Sato, Shoji, and Ota 1959), 
perhaps adapted to the environment, grew better in the dark than in the 
light; red light depressed the mycelial growth rate of an isolate of B. cinerea 
(Rabinovitz-Sereni 1932), as did continuous, near-ultraviolet irradiation (Tan 
and Epton 1973). By contrast, orange light stimulated the germination of 
conidia in B. cinerea (Chebotarev, Lanetskii, and Naberezhnykh 1968; Zem- 
lyanukhin 1973). 

The absorption of energy by B. cinerea irradiated by visible and ultra- 
violet light was investigated by Zemlyanukhin and Chebotarev (1973). 

The effect of light in enhancing sporulation of Botrytis spp. has long 
been known from the work of Reidemeister (1909), Paul (1929), Rabinovitz- 
Sereni (1932), and Harada, Takashima, Fujita, and Terui (1972). Usually, 
few conidia of B. cinerea are formed in the dark or in red light. 

Harada, Takashima, Fujita, and Terui (1972) found that a 12-h dark 
cycle or continuous light promoted sporulation and suppressed sclerotial 
formation in B. cinerea; no sclerotia were formed in continuous light intensi- 
ties exceeding 500 Ix. 

Page (1956) considered that the mycelial growth of Botrytis squamosa 
was arrested by light from incandescent and fluorescent sources and that con- 
centric rings of sclerotia formed on Czapek agar were a sequel to alternating 
darkness and light. Stinson, Gage, and MacNaughton (1958), however, sus- 
pected that Page's results could be interpreted in terms of temperature effects 
and found that B. squamosa could withstand exposure to a light intensity of 
100 ft-c for several days and to 250 ft-c for a few hours. Bjornsson (1956, 
1959) noted a similar concentric ridging of mycelial growth in cultures of 
B. gladiolorum on potato dextrose agar at 21 °C. 

Beck and Vaughan (1949) found that B. cinerea parasitizing Saint paulia 
sporulated profusely in conditions of low light intensity and Melchers (1926) 
noted that bright sunlight reduced sporulation of B. cinerea on geranium. 

Beaumont, Dillon Weston, and Wallace (1936) exposed cultures of B. 
tulipae to sunlight to induce sporulation and Leach (1961, 1962), Leach and 
Tulloch (1972), Schlosser (1970), and Kite (1971, 1973^) found that near- 
ultraviolet radiation induced prolific sporulation in cultures of B. cinerea, in 
common with many other fungi; ever since, exposure to light, especially near- 
ultraviolet light, has become a standard practice for inducing sporulation in 
all species. Leach's technique was to illuminate cultures in Pyrex glass con- 
tainers at 76-740 ^Wcm"^ and 21 °C with light of wavelength 320-380 nm. 

Tan and Epton (1973) found that infrared, red, and yellow light stimu- 
lated the sporulation of B. cinerea only slightly and blue and green light not 
at all. This contrasts with the blue light stimulation of sporulation in B. 
gladiolorum (Bjornsson 1956, 1959). 

The photoreception system in B. cinerea was found by Tan and Epton 
to be extremely sensitive to near-ultraviolet light; a single exposure of 1 min 

36 



at 151 fiWcm - in the most sensitive phase (the culture aged 4-5 days) was 
sufficient to induce sporulation but continuous irradiation was inhibitory. 
Like Pieris (1947), Tan and Epton found that the age of the culture is 
critical in the light response; cultures older than 10 days become unresponsive. 
The receptor system of B. cinerea evidently can receive blue light as well as 
near-ultraviolet and red light but Tan and Epton could not suggest what the 
system might be. 

Tan and Epton (1974) next showed that the inhibition of sporulation by 
continuous irradiation in the wavelength range 300-420 nm is temporary and 
that the blue component is probably responsible because the sporulation 
response induced by near-ultraviolet is partially reversed by blue light. This 
reversal is nullified by further exposure to near-ultraviolet. They postulated 
the existence of the near-ultraviolet and blue photoreceptor mycochrome 
(Honda 1969) in B. cinerea. 

Tan (1974fl) next showed that 12 h after the sporulation response was 
induced by near-ultraviolet irradiation, blue light in an exposure of 15 min at 
250 /xWcm~2 gave 20% suppression of sporulation of B. cinerea. There were 
2 phases of maximum sensitivity to blue-light inhibition of sporulation, one 
12-16 h after induction by near-ultraviolet and the other at 20-24 h. The 
inhibition response reached a maximum at 60% inhibition of sporulation 
after 6 h of blue-light irradiation. Spore formation was arrested and dediffer- 
entiation of conidiophores to sterile hyphae began. 

Tan suggested that blue light might convert the Mb form (effective for 
sporulation) of the hypothetical mycochrome to Mxuv, the form that is not 
effective for sporulation but is effective in the formation of sterile, erect 
hyphae instead of conidiophores. Mn,jv is converted back to Mb by near- 
ultraviolet light and by darkness. Blue-light inhibition of sporulation is repeat- 
edly photoreversible (Tan 19746), especially by red and far-red irradiation. 
This reaction suggested to Tan that phytochrome or some other pigment 
system was involved. 

Hite (1973/?) demonstrated the presence of a sporogenic substance — 
coded P310 because it has an absorption peak at 310 nm (Trione and Leach 
1969) — only in sporulating mycelia and sporulating sclerotia of B. cinerea 
irradiated with near-ultraviolet light. P310 was absent from nonsporulating 
sclerotia despite near-ultraviolet irradiation. 

Requirements for sclerotial production are generally the opposite of 
those for sporulation; regular diurnal light inhibits sclerotial formation in 
B. cinerea (Reidemeister 1909; Paul 1929; and Vanev 1966) and in B. squa- 
mosa (Page 1956), but a Ught stimulus was reported to be necessary in B. 
gladiolorum (Bjornsson 1956, 1959). Tan and Epton (1973) found that B. 
cinerea formed sclerotia in darkness, in yellow, red and infrared light, and 
when irradiated for less than 30 min with near-ultraviolet light. 

Both visible and ultraviolet light affected the activity of various extra- 
cellular enzymes of B. cinerea (Zemlyanukhin and Chebotarev 1972). 

37 



Light is essential for the full development of the ascigerous disc in 
apothecia of Botryotinia ricini (Godfrey 1923) and of B. squamosa (Bergquist, 
Horst, and Lorbeer 1972; Bergquist and Lorbeer 1968, 1972) and other 
species probably also have this requirement, which is common in other genera 
of the family. 



Phototropism 

Negative phototropism was first noted in the germ tubes of a Botrytis 
sp. by Robinson (1914) and confirmed in those of B. cinerea by Gettkandt 
(1954) using daylight and incandescent lamps of about 200 Ix as light sources 
and by Jarvis (1972) using near-ultraviolet fluorescent illumination. In all 
cases, the majority of germ tubes were oriented in the direction of incident 
light on gelatine or agar plates illuminated from the side. Only short-wave- 
length light is effective (Biinning and Etzold 1958; Jarvis 1972). Gettkandt 
could find no carotenoid pigment or other possible photoreceptive pigment in 
the spores or germ tubes, but Banbury (1959) thought that the photoreceptor 
riboflavin was probably present in the tips of the germ tubes of B. cinerea. 

Positive phototropism was noted in the stipe of the apothecium of 
Botryotinia ricini by Godfrey (1923) and of B. fuckeliana by Gettkandt. 

Jarvis (1972) found the conidiophores of B. cinerea to be positively 
phototropic when grown on a dilute soil extract agar plate, illuminated from 
the side by near-ultraviolet lamps to induce sporulation (Leach 1962). By 
rotating the plates through 45°, 90°, etc. in the same horizontal plane, the 
conidiophores could be induced to change direction, so that they continued 
to grow towards the light. Within a limited range of Wratten filters and with 
the same illumination, the maximum phototropic effect was obtained with 
the filter transmitting light of a wavelength around 420 nm, less effect around 
440 nm and the least effect around 480 nm. No phototropism was found 
when the light passed green, yellow, orange, or red filters. 

When conidia of B. cinerea were illuminated from vertically above with 
plane-polarized light, Biinning and Etzold (1958) found that the germ tubes 
were oriented parallel to the plane of polarization in either direction from the 
spore. Only short-wavelength light of less than 500 nm was effective. By 
turning the agar plates through 45°, the direction of growth of the young germ 
tubes could be changed. 

Interposing a doubly-refracting polarizer between the conidia and the 
first polarizer gave light differing in wavelength by 225-230 nm and 
polarized in directions 45° apart and resulted in germ tubes growing per- 
pendicular to the initial direction. These results led Biinning and Etzold to 
postulate that a yellow photoreceptive pigment is in doubly-refracting 
dichroic structures, probably near the cell membrane and this hypothesis 
received further support from Jaffe and Etzold (1962) studying the germina- 
tion of conidia of B. cinerea in blue light of about 470 nm. They deduced that 

38 



the photoreceptors were highly dichroic and oriented anticlinally within the 
inner half of the cell wall. In plane-polarized light, the germ tubes emerge 
from the areas of maximum light absorption. 

Nothing is known of the photoreceptive mechanism in the conidiophore 
of Botryds cinerea or in the stipe of Botryotinia juckeliana or of B. ricini. 

B. cinerea in culture was killed by radiation of 5.6 m wavelength 
(Metlitski and Soboleva 1936) and 8-40 m and 5.2-10 m wavelengths 
(Treveskoy 1937) probably as the result of high temperatures induced in the 
substrate. 



Effects of pH 

Webb (1921) found that conidia of Botryds cinerea germinated over a 
very wide range of pH, from 1.6 to 6.9 on mannite and from 2.0 to 9.8 on a 
sugar beet decoction; the optima ranged between 3.0 and 7.0 depending on 
the medium. At pH 2.1, germ tubes were abnormal in appearance and below 
this they began to disintegrate. Vanev (1965) gave the pH range for growth 
of B. cinerea as pH 2-8 (-8.5) with an optimum around 3-5. Sclerotia are 
formed best at pH 4 and not at all in alkaline media (Vanev 1966). 

The pH changes induced by B. cinerea in culture depend on the medium; 
Weimer and Harter (1923) found an isolate to induce a final pH of 2.5 in a 
Czapek solution, but an alkaline reaction in a potato decoction. 



Effect of age and nutrition 

The germinability of conidia of B. cinerea depends in part on the age of 
the culture (Brown 1922c; Singh 1940). Conidia taken from very young 
cultures, perhaps when immature, and those taken from old cultures, perhaps 
when senescent, germinated relatively slowly while those from cultures of 
medium age (16 days) germinated fastest. A similar relation held for the rate 
of germ tube growth. The addition of an extract of lentils as an exogenous 
source of growth substances, including biotin and thiamine, considerably en- 
hanced the germination and germ tube growth of young conidia. Conidia 
contained an endogenous source of growth substances if taken from a culture 
grown on a medium augmented with lentil extract and germinated better than 
those taken from a medium not so augmented (Singh 1940). Similarly, 
Shiraishi, Fukutomi, and Akai (1970^) were able to restore the germinative 
ability of aged conidia of B. cinerea by supplying them with mono-, oligo-, or 
polysaccharides at concentrations of the order of IO-2 M, or 10-3 M, but 
not 10"5 M. In decreasing order of effectiveness were glucose, fructose, 
sucrose, maltose, lactose, dextrin, inulin, and starch. 

It has long been known that the germination of conidia of Botryds spp. 
in infection drops is enhanced by the addition of plant extracts (Brooks 

39 



1908; Brown 1916, \922a; Wilcoxon and McCallan 1934; Kovacs and 
Szeoke 1956; Kosuge and Hewitt 1964; among many others). Hawker (1950) 
distinguished between the effect of nutrients on germination and those on 
germ tube growth. Thus, for example, conidia of B. cinerea germinated more 
slowly in 3% malt extract or undiluted turnip extract than in water or dilute 
extracts, though the proportion germinating was higher and eventually the 
germ tubes were longer in the undiluted extracts. 

Kosuge and Dutra (1962) found that the conidia of an isolate of 
B. cinerea germinated very poorly in water, but well in a medium containing 
L-serine, D-glucose, and sodium acetate, each at 0.002 M, and buffered at 
pH 5.2. Oxygen uptake during germination was enhanced in the medium when 
serine and aspartic acids, the main components of the free amino acid pool 
in ungerminated conidia, were readily metabolized. When the conidia were 
germinated in the presence of (^^C) bicarbonate, the labelled carbon appeared 
in aspartic acid and 2 other unidentified compounds. 

Chou (1972) also failed to germinate conidia of B. cinerea in water, in 
solutions of aspartic or glutamic acids, or in solutions of growth substances 
(gibberellic acid, indole-3-acetic acid or kinetin). Solutions of more than 
100 ppm glucose, fructose, or sucrose, however, permitted germination. 

Sztejnberg and Blakeman (1973^) showed that the supply of necessary 
nutrients on beetroot leaves to germinating conidia of B. cinerea was probably 
controlled by the other epiphytic microflora, especially bacteria with copious 
polysaccharide sheaths, an effect simulated by nutrient-leaching treatments. 
Borecka and Millikan (1973) demonstrated that the presence of pollen grains 
of many species enhances the germination of spores of B. cinerea. 

Botrytis cinerea can be grown in solutions of high osmotic pressure; 
Hawkins (1916) found it grew in solutions of 4.75 X 103 kNm - and 
Rippel (1933«) germinated conidia of B. cinerea and of a Botrytis sp. in 1.0 
M, 1.3 M, and 1.96 M sucrose solutions (3.50 X 103, 6.66 X 103, and 
1.03 X 10^ kNm - respectively). There was a direct correlation between the 
rate of germination and osmotic pressure. 

Another important factor in spore germination is spore concentration. 
Brown (1922c) and Schiitt (1971/?) found that the optimum concentration for 
germination varied with the isolate of B. cinerea; two of three isolates had 
an optimum concentration of 127 X 103 spores/ml, the third 65 X 103 
spores/ml. 

The sporulation of B. jabae in culture is promoted by relatively high 
concentrations of inorganic salts or very high concentrations of glucose 
(Leach and Moore 1966). This species does not sporulate on host leaves until 
they are almost desiccated, and Leach and Moore interpreted these results 
in terms of a high osmotic pressure requirement for sporulation. 

Sporulation of B. convoluta was generally most profuse on media which 
supported maximum growth (Maas and Powelson 1972) and was inhibited 
by sorbose, glycine, or urea and on media lacking a carbon or nitrogen source. 

40 



The germination, growth, and sporulation of the speciahzed Botryotinia 
ricini was found by Orellana and Thomas (1964) to be considerably enhanced 
by the addition of 0.4% gallic acid and 1 % glucose to the medium. 

Sclerotial formation is also considerably influenced by nutrition and 
especially by the ratio of carbon to nitrogen supplied. Townsend (1957) 
recognized, however, that sclerotia of B. cinerea and of B. allii are initiated, 
develop, and mature in three distinct stages, each with a different set of 
nutritional requirements. A high carbohydrate and, to a lesser extent, a high 
nitrogen concentration favors sclerotium initiation, but the amounts permit- 
ting initiation do not always permit full maturation as judged by full pig- 
mentation. This last stage does not begin until mycelial growth is checked 
by nutrients becoming unavailable or possibly by a qualitative change in 
metabolism. Thus when large numbers of sclerotia are initiated, some fail to 
mature. The fact that manipulation of the C:N ratio determines whether 
sclerotia or conidia are formed suggested to Hawker (1950) that the two 
types of growth are induced by different metabolic sequences. 

Sclerotia of B. cinerea develop best on rich media in high relative 
humidity and in the dark (Reidemeister 1909; Paul 1929; Vanev 1966; and 
Harada, Takashima, Fujita, and Terui 1972), requirements opposite to those 
for sporulation. Pieris (1947) found that sclerotial formation by B. cinerea 
was favored by a high carbon: nitrogen ratio in the nutrients supplied. Town- 
send (1952) and Vanev (1966) confirmed this and showed that sclerotial 
production increased in proportion to the amount of sucrose supplied; glu- 
cose, fructose, or maltose were suitable substitutes for sucrose. Valaskova 
(1963«) also found a rich carbohydrate supply to favor sclerotial production 
by B. tulipae. 



Staling 

Hawker (1950) classified Botrytis cinerea as a non-staling organism 
because it does not produce concentric zones of poor or abnormal growth in 
cultures that result from the local accumulation of growth-inhibiting metab- 
olites. It is, however, sensitive to the staling products of some other organisms, 
for example Fusarium spp. (Lutz 1909; Pratt 1924(3, 1924Z>; and Boyle 1924). 
Inhibitors include potassium bicarbonate, fatty acids, and thermo-labile 
materials. 

On the other hand, Hawker (1936) showed that culture liquids staled by 
prolonged growth of B. cinerea contain inositol, which stimulates sporulation 
in Melanospora (Sordaria) destruens. 

Lahoz, Ballesteros, and Gonzalez (1971) demonstrated changes in 
polyol concentration in autolysing cultures of B. cinerea. 

Other species of Botrytis, for example B. squamosa, form sclerotia in 
concentric rings in culture (Page 1956); this formation may result from 

41 



staling, but has been interpreted in terms of light and temperature effects 
(Stinson, Gage, and MacNaughton 1958). 



Effects of volatile metabolites 

When Carlile and Sellin (1963) placed conidia of Botrytis cinerea on 
cellophane over colonies of the fungus, germination was inhibited but 
proceeded normally when the fungus was removed. Germination was 
similarly inhibited by colonies of Aspergillus niger, Penicillium notatum, and 
Chaetomium globosum. 

Dick and Hutchinson (1966) also noted inhibition of growth and 
sporulation of B. cinerea on cellophane when placed over cultures of 19 
other fungi, 8 of which decreased sporulation by more than 25%. They 
attributed inhibition to the effects of volatile fungal metabolites but they also 
found 5 fungi that stimulated B. cinerea and 38 others that had no effect. 

In fruit and vegetable stores, B. cinerea was sensitive to acetaldehyde, 
ethyl acetate, and other volatile metabolites (Aharoni and Stadelbacher 1973; 
Prasad, Stadelbacher, Shaw, and Aharoni 1973). 



Effects of atmospheric gases and pollutants 

Although Doran (1922) noted that conidia of Botrytis cinerea ger- 
minated better on the surface of water drops than in the interior and inter- 
preted this in terms of oxygen supply. Brown (1922c) found that conidia of 
B. cinerea were relatively insensitive to a wide range of concentrations of 
oxygen. Follstad (1966) noted a decrease in mycelial growth rate with de- 
creasing oxygen supply, and complete suppression of sporulation by con- 
centrations below 1%. Similarly, Adair (1971) found that oxygen concentra- 
tions below 1.7% decreased the radial growth rate of B. cinerea on agar, and 
that gray mold rot in stored cabbage was adequately controlled in a concen- 
tration of 1.4%. 

Wells and Uota (1969) found that mycelial growth of B. cinerea in a 
liquid medium decreased linearly with decreasing oxygen concentration 
below 4%. 

Brown (1922c) found that the germination of spores of B. cinerea was 
inhibited at 20-30% CO2 when in water, but a higher concentration, above 
50%, was required to inhibit germination when in dilute turnip extract. 
Temperature and other physiological factors were also important in deter- 
mining the effect of CO2, and Brown concluded that the retarding effects of 
CO2 are greatest when the energy of growth (sic) is lowest in unfavorable 
conditions for germination and growth. Wells and Uota obtained 90% 
inhibition of germination in 16% CO2 at 19°C and Rippel and Heilmann 
(1930) found considerably enhanced growth of Botrytis sp. from sunflower 

42 



at increasing concentrations of CO2 up to 0.1%; thereafter growth was in- 
creased only slightly by concentrations up to 1 % . 

The sporulation of B. allii (B. aclada) was retarded in an atmosphere 
of 2% CO2 and 2% O2 (Littlefield, Wankier, Salunkhe, and McGill 1966) 
and though the height of the aerial mycelium was reduced, the radial growth 
was unaffected. In 10.5% CO2 and 2% O2, sporulation was inhibited and 
growth retarded in height and radial extension. 

When the partial pressure of oxygen was reduced by Wu and Salunkhe 
(1972) to 102 mm of mercury (about 0.13 bar) in a gas mixture of 2.7% O2 
and 97.3% N2, mycelial growth of B. aclada was reduced to about 90% of 
the growth in a laboratory air atmosphere (646 mm of mercury), and the 
sporulation rating reduced from 8 to 7. At subatmospheric air pressures, 
growth and sporulation were progressively delayed and reduced at 278 mm 
and 102 mm, but not at 471 mm of mercury. 

Of pollutants, ozone is fungistatic to B. cinerea in concentrations as low 
as 0.5 ppm, although very low concentrations stimulated germination of 
conidia (Magdycz 1972). A successful pilot attempt to use ozone in con- 
trolUng gray mold in stored strawberries was made by Spalding (1966). 
Aerial mycelium was almost completely absent but stromatic tissue was 
formed in an atmosphere containing 2 ppm. On removal from the ozone, 
this tissue resumed growth. Magie (I960) also used ozone to control B. gla- 
diolorum in picked Gladiolus flowers but Manning, Feder, and Perkins 
(1972) failed to control B. cinerea on poinsettia flowers and bracts with ozone. 

Ozone at 100 and 50 ppm reduced the germination of conidia of B. allii 
(B. aclada) and colonies showed abnormal growth (Hibben and Stotzky 1969). 
There was little effect, however, on air-dried spores or on those suspended in 
liquid media. 

An unusual effect was noted by Magdycz and Manning (1973): B. 
cinerea protected broad beans from ozone injury. 

Although the effects of sulfur dioxide as an atmospheric pollutant on 
Botrytis spp. have not been investigated, SO2 has been widely used to con- 
trol gray mold in stored grapes, raspberries, strawberries, and black currants 
(Harvey and Pentzer 1960; Nelson 1973; Cappellini, Stretch, and Walton 
1961; and Jarvis 1967). Couey and Uota (1961) found that the effectiveness 
of SO2 in inhibiting conidial germination in B. cinerea increased with in- 
creasing relative humidity; at 96% RH a given concentration of SO2 was 
20 times more effective than at 75% RH. Between 0°C and 30°C, the Oio 
value was 1.5. The reduction in percent germination was directly propor- 
tional to SO2 concentration and to exposure time. 

McCallan and Weedon (1940) compared the toxicities of SO2, HCN, 
HgS, CI2, and ammonia to the conidia, mycelium, and sclerotia of B. cinerea 
and of some other fungi. SO2 and CI2 were the most toxic, H2S and HCN 
the least toxic, and ammonia was intermediate. 

43 



Autotropism 

When spores of Botryds cinerea germinate close together in pairs, the 
germ tubes tend to emerge from adjacent areas and to grow towards each 
other. Jaffe (1966) analyzed many such pairs of spores germinating in a thin 
layer of Czapek-Dox broth in air, and termed the phenomenon autotropism. 
The majority of germ tubes emerged on the same side of a line joining the 
centers of adjacent spores, a cis arrangement, as opposed to the trans arran- 
gement where germ tubes emerged on opposite sides of the line. There was 
also a tendency for the second emerging germ tube to be + (growing towards 
its neighbor) if the first germ tube was + (a + + arrangement) and for 
the second germ tube to be — if the first germ tube was — (a arrange- 
ment). There were relatively few -\ — pairs. JalTe interpreted his results to 
mean that there was an emission of a diffusible, unstable, locally effective, 
macromolecular stimulant. In an atmosphere staled by fungal growth and 
containing 17.5% Oo and 4.5% CO2, there was a striking reversal of auto- 
tropism. Only 9% of the pairs were + + compared with 92% in laboratory 
air, and there was a reduction in the cis tendency from 92% to 72%. When 
the laboratory air was enriched with 0.3% or 3% CO 2 there was again re- 
versal of autotropism, and Jaffe postulated that in higher CO2 atmospheres, 
spore pairs were dominated by a locally effective, but uniformly emitted 
inhibitor, although the stimulator continued to have some effect. Altering the 
pH of the system had no effect. 

Robinson, Park, and Graham (1968) confirmed Jaffe's results but found 
that spore pairs were neutrally autotropic on agar, though still predominantly 
cis. However, on cellophane on agar, on which germ tubes were in one plane 
as in thin layers of broth, spore pairs were again + + and cis. In H — pairs, 
there was a strong tendency for germ tubes to curve away from each other. 

Though in semi-isolated spore pairs there was a tendency for each germ 
tube to be in line with the major axis of its spore, it was not considered to 
contribute to autotropic effects. Robinson et al. found that Jaffe's postulated 
factors diminish markedly in effect with increasing distance between spores, 
and the effect was hardly demonstrated at distances greater than 50 /^m. 

Autotropism is reviewed by Robinson (1973). 



Rheotropism 

Jonsson (1883) proposed the term 'rheotropism' to apply to the direc- 
tional growth of young hyphae of B. cinerea downstream and of old hyphae 
upstream when the culture medium was flowing past the thallus. Much later, 
MUUer and Jaffe (1965) found that when spores of B. cinerea, sparsely sown 
and hence largely independent, were fixed to the wall of a laminar flow 
chamber and subjected to a flow of a dilute nutrient broth, most of the germ 
tubes grew downstream. The rate of germination fell so slowly with increasing 
flow rate of the medium as to suggest the localization of a growth stimulant 

44 



and Miiller and Jaflfe (1965) considered that this rheotropic response is 
mediated by convection across each cell of a diffusible stimulator emitted by 
the cell. They deduced that the stimulator is macromolecular and has a 
diffusion constant of about 10""cm-sec"i and a half-life of about 10 sec. 
Dark-grown cells were slightly less oriented by flow. 



Sporulation inhibitors 

A number of materials, mostly chelators and mitotic inhibitors, spe- 
cifically inhibit sporulation of a number of fungi including B. cinerea, but 
copper salts and a,;S-unsaturated ketones enhance spore differentiation, 
possibly, suggested Horsfall and Rich (1959), by reversing the action of some 
natural inhibitor, which could be a sulfydryl compound. Thus the inhibitory 
action of ethylenebenzene-2-thiol is reversed by an a, ^-unsaturated ketone, 
pulegone, and by copper sulfate. Also inhibiting sporulation and similarly 
reversed is 2- (7-trichloropropyl) benzothiazole. Horsfall and Rich (1960) 
also found sporulation in B. cinerea to be inhibited by 1, 1,1, 3,3,3, 3-hexa- 
chloro-2-propanol incorporated into nutrient agar at 50 and 1 00 ppm; although 
clavate conidiophores were formed, they bore no conidia. Unlike trichloro- 
benzothiazole, hexachlor-2-propanol also bleached the black pigments of the 
fungus. Its 1,3-dichloro- analogue was only weakly active and the ketone 
tautomer was inactive, indicating that its OH" group is the site of activity. 
Hexachlor-2-propanol is cheap and easy to manufacture, and Horsfall and 
Rich (1960) suggested that it could be added to control programs. It was 
added to standard captan spray programs (Jarvis 1962e), and some slight 
improvement was indeed obtained in the control of strawberry gray-mold. 

Tecnazene, a fungicide widely used in lettuce cultivation for the control 
of gray mold, is believed to be effective mainly because of its antisporulant 
activity (Reavill 1950, 1954). 



Storage 

The sclerotia are commonly regarded as food storage organs for sur- 
vival; those of B. cinerea were reported to contain 68-73% water, 2.5% 
nitrogen, 0.5% reducing sugars, 0.7% non-reducing sugars, and 2.7% lipid 
material (Townsend 1952). The lipid content may vary with the source of 
sclerotia; those of B. tulipae collected from the host by Sumner and Colotelo 
(1970) had 3.3% by dry weight, and those from culture had 2.9%. Further, 
the component fatty acids, mainly palmitic, oleic, linoleic, and a-linolenic 
acids, tended to be more unsaturated in sclerotia from the wild. Haskins, 
Tulloch, and Micetich (1963) found the mycelium of an isolate of B. cinerea 
to have an oil content of 2.6% and a fatty acid composition mainly of 
palmitic, oleic, linoleic, and a-linolenic acids, the last amounting to 9.4% 
of the fatty acid fraction, compared with 41.7% reported from another 
isolate of B. cinerea (Shaw 1965) and with less than 5% in sclerotia of 

45 



B. tulipae (Sumner and Colotelo 1970). Shaw considered that the presence of 
7-linolenic acid differentiated Phycomycetes from all other fungi, and that 
the inter-isolate differences in a-linolenic acid may be associated with taxo- 
nomic differences in the genus Botrytis. 



METABOLISM 



All Botrytis species are relatively easy to grow in culture on a wide 
range of synthetic and natural media, and all are aerobes. 



Selective media 

Netzer and Dishon (1967), Lorbeer and Tichelaar (1970), Ellerbrook 
and Lorbeer (1972) and Barkai-Golan (1973) devised a few selective media, 
mostly ones that exploit interspecific differences in fungicide tolerance. 



Carbohydrates 

The metabolism of carbohydrates by B. cinerea has received most atten- 
tion in the field of enology (q.v.). In general, B. cinerea is able to utilize 
most sugars but an isolate of B. cinerea used by Fraser (1934) was unable 
to utilize pentoses, mannose or lactose and it failed to grow on raffinose. 

Stadler (1954) found that B. cinerea grew poorly on /-rhamnose and 
inulin but it was able to utilize some glycosides, namely, in order of descend- 
ing utilization, amygdalin, aesculin, arbutin, salicin, digitalin, and saponin. 

Smirnov, Kostik, Todirazh, Mazur, and Mogilenko (1972) found that 
B. cinerea could utilize maltose, starch, and several related substances. 
Botrytis convoluta utilized, with decreasing ability, maltose, glucose, starch, 
galactose, and fructose, but not lactose or sorbose (Maas and Powelson 1972). 

The ability of Botrytis species, with the possible exception of B. con- 
voluta (Maas and Powelson 1972), to degrade cell-wall materials is of pro- 
found importance in pathogenesis; and the activity of pectinases, cellulases 
and cutin-esterase in this respect is discussed elsewhere. The in vitro produc- 
tion of pectinases has been studied in detail, notably by Brown and his stu- 
dents over a number of years (Brown, 1915, 1917, 1934, 1936, 1955) and 
others, including Davison and Willaman (1927), Vasudeva (1930«), Gau- 
mann and Nef (1947), Ashour (1948), Jermyn and Tomkins (1950), Damle 
(1951), Jarvis (1953), Winstead and Walker (1954), Wood (1960), Deverall 
and Wood (1961a, 1961/?), Thomas and Orellana (1963Z)), Hancock, Miller, 
and Lorbeer (1964), Kaji, Tagawa, and Yamashita (1966), Sherwood (1966), 

46 



Tani and Nanba (1969), Smirnov (1972), Urbanek and Zalewska (1973), 
Verhoeff (1973), Verhoeff and Warren (1972), and Shishelova and Fedorova 
(1974). 

The enzymes include pectin methylesterase, polygalacturonase, and pec- 
tin- and polygalacturonate-methyl-rrfl^^-eliminase, and are reported from 
B. cinerea, B. allii (B. aclada), B. squamosa, B. fabae, and B. ricini; each 
species probably produces some or all of the enzymes, both exogenously and 
endogenously, because all species except perhaps B. convoluta attack cell 
walls in characteristic soft rots. In general, pectinases are readily produced 
on simple media containing a carbohydrate, a nitrogen source, and simple 
salts. Gaumann and Bohni (1947) found that polygalacturonase was a 
constitutive enzyme of B. cinerea, whereas, as Zalewska, Rochowska, and 
Urbanek (1970) also demonstrated, pectin methylesterase was adaptive and 
its activity in culture filtrates largely depended on the presence of pectin. 

Verhoeff and Warren (1972) detected pectin methylesterase and endo- 
and exopolygalacturonase activity in media containing germinating spores of 
B. cinerea, and, at some temperatures, endopolygalacturonase activity before 
germination. Some endo- and exopolygalacturonase activity was detected in 
water used to wash the spores. Verhoeff and Warren thought that all the 
enzymes were adaptive. 

The role of pectinases in pathogenesis is more fully discussed in PART 
4, "Pathogenesis". There is no doubt however that these enzymes also play 
a considerable role in the saprophytic degradation of plant tissues above and 
below the ground (Peltier 1912); see PART 1, "Introduction". 

Pectic materials of all types and of all degrees of methylation are readily 
utilized as carbon sources. 

Cellulose is also utiHzed by B. cinerea (Lyr and Novak 1962; Kohlmeyer 
1956; Hancock, Millar, and Lorbeer 1964; Lapsker, Trofimenko, and 
Al'man 1973), by B. allii (B. aclada) and B. squamosa (Hancock et al. 1964) 
and by a Botrytis sp. in soil (Felsz-Karnicka 1936). In Kohlmeyer's study, 4 
isolates of B. cinerea from different host genera produced different amounts 
of cellulase. On cellulose hydrate discs, the isolates caused grooves but no 
penetration of a membrane 0.04 mm thick, although each was able to degrade 
natural cellulose from sunflower and elder pith. Deverall and Wood (1961!?) 
and Verhoeff and Warren (1972) also detected cellulase activity by B. cinerea. 
Cellulase is probably important to the saprophytic rather than to the parasitic 
activity of Botrytis species. 

Other enzymes from B. cinerea capable of degrading cell-wall materials 
have been investigated in vitro; they include hemicellulase, xylanase, and 
mannanase (van Parijs 1961; and Lyr and Novak 1962), and arabanases 
were reported from B. allii (B. aclada), B. tulipae, and B. fabae by Fuchs, 
Jobsen, and Wouts (1965). 

In B. cinerea, Ampuero (1966) found an inverse relation between sugar 
utilization and mycelial growth inhibition by nystatin and phleomycin. This 

47 



relationship may be connected with the effect of griseofulvin on the proper 
construction of the cell wall of B. cinerea (Gottlieb and Huber 1965) and of 
B. alia (B. aclada) (Evans and White 1967). Similar distortions were noted 
in germ tubes of B. cinerea treated with benomyl (Richmond and Pring 
19716). Barathova, Betina, and Nemec (1969) found that 29 of 31 anti- 
biotics they examined inhibited the growth of B. cinerea and of these, 20 
induced abnormalities of hyphal growth. Betina, Micekova, and Nemec 
(1972), Betina, Micekova, and Daniela (1973), and Fassatiova (1972) ob- 
served similar effects of cytochalasins on B. cinerea. A mixture of sclareol 
and 13-epi-sclareol (diterpenes from the leaf surface of Nicotiana glutinosa) 
did not inhibit germination of B. fabae, but affected radial growth by their 
griseofulvin-like effect on hyphal branching (Bailey, Vincent, and Burden 
1974). Another antibiotic, roseofungin, had a similar effect (Nikitina and 
Kazakova 1972). 

The utilization of carbohydrates by B. cinerea, particularly in higher 
concentrations, has been extensively investigated by Kamoen (1964, 1966) 
and carbohydrate metabolism in relation to the production of oxalic acid 
(of controversial role in pathogenesis; q.v.) by Jamart and Kamoen (1972) 
and Gentile (1954). Gentile proposed a Krebs-cycle system: glucose ■*- gluconic 
acid -^ phosphogluconate — pentose phosphate-^ triose phosphate -► pyruvate -*- 
malate ■*■ oxalate, the last stage by direct oxidation. 

In an attempt to utilize enzymes from B. cinerea in the commercial 
production of sweet wines (see PART 4, "Enology"), de Jong, King and 
Boyle (1968) examined some of the other enzymes involved in carbohydrate 
metabolism. Glucose-6-phosphate NADP dehydrogenase was active and an 
NADH-sensitive phenol oxidase was implicated in a decolorizing action on 
the wine. 

The calorific value of the cell contents of hyphae of B. cinerea in 
culture on potato dextrose agar was found by de Soyza (1973) to be about 
3.5 kcal/g ash-free wt. 



Nitrogen 

B. cinerea was among a number of fungi reported by Nilova, Egorova, 
Rashevskaya, and Kozhevnikova (1964) to fix atmospheric nitrogen. Protein 
accumulated both in the mycelium and in the medium, and fixation was 
stimulated by ammonium salts. Morton and Broadbent (1955) demonstrated 
the formation of extracellular nitrogen compounds by B. allii (B. aclada) in a 
medium containing ammonium sulfate. The new material was mostly peptide 
that the fungus was unable to utilize, although on hydrolysis it yielded 14 
amino acids that were utilized. 

The growth of B. cinerea was significantly correlated with nitrogen level 
when grown in nitrate- and phosphate-containing media (Dowding and Royle 
1972). Although nitrate assimilation was almost always complete, that of 

48 



phosphate was not, especially in low-nitrate media. After nitrogen incorpora- 
tion into mycelia, only 10% was available for incorporation into conidia, 
but 40% of the phosphate was available. 

All species of Botrytis can utilize a wide range of nitrogenous materials, 
from nitrites and nitrates to hydrolysates of casein and similar materials, 
although there are differences between species. Thus, for example, Hacskaylo, 
Lilly, and Barnett (1954) and Maas and Powelson (1972) found B. cinerea 
and B. convoluta to respond poorly and well, respectively, to ammonium 
nitrogen as compared with nitrate nitrogen. Stadler (1954) found asparagine 
to be the best, and potassium nitrate the poorest, source of nitrogen for 
B. cinerea and there were interactions between acid and nitrogen. 

Of recurring interest in physiological work has been the effect of the 
carbon : nitrogen ratio. It affects pectinase production (see above) and the 
type of growth, sclerotial production, sporulation, etc. (Pieris 1947; Hawker 
1950; Townsend 1952, 1957; Valaskova 1963^; Kamoen 1964, 1966; for 
example); such changes are usually the result of shifts in pH of systems. 



Amino acids and proteins 

The uptake and accumulation of amino acids by B. fabae was studied 
by Jones (1963); L- and D-isomers both accumulated, the former more 
rapidly. The uptake mechanism was dependent on unsubstituted — NH2 and 
■- COOH and was inhibited by uncouplers of oxidative phosphorylation. 

Some synthetic analogues of amino acids, purine and pyrimidine marked- 
ly depressed the growth rate and enzyme production in cultures of B. cinerea 
(Urbanek and Zalewska 1973). 

Zemlyanukhin and Chebotarev (1971) found that light had a marked 
effect on amino acid metabolism; free lysine, serine, alanine, tryptophane, 
valine, methionine, and leucine all increased in the mycelium of B. cinerea 
exposed to red, yellow, or violet light, but glutamic acid decreased. Exposure 
to ultraviolet Hght increased the accumulation of all amino acids at least 
fourfold, and that of tryptophan about 40-fold. Zemlyanukhin, Chebotarev, 
and Tsiomenko (1971) found that ultraviolet Hght at 36 mWcm"2 in a 30- 
min exposure destroyed protein, but amino- and C3 acids accumulated in the 
mycelium and in the medium. 

The cytostat 1,6-dibromo-D-mannitol was shown by Szabo, Holly, Hor- 
vath, and Pozsar (1972) to effect an increase in protein nitrogen in the myce- 
hum of B. cinerea, sometimes by as much as 20%, possibly by DNA induc- 
tion. 

Lyr and Novak (1962) reported amylase and proteinase activity in 
cultures of B. cinerea and Ovcarov (1938) reported an endogenous de-urease 
in B. cinerea, which split off urea from protein, in this case, gelatine, and this 

49 



enzyme was considered to be of considerable importance in nitrogen metab- 
olism. Smirnov, Kostik, Todirash, Mazur, and Mel'nik (1972) and Astapo- 
vich, Babitskaya, Hrel, and Vidzischchuk (1972) detected peptolytic enzymes 
in B. cinerea. Tseng and Lee (1969) reported the production of a proteolytic 
enzyme by B. cinerea in vitro that was active over the pH range 5-8.5, with 
its optimum at the higher value. Trofimenko and Shcherbakov (1973) found 
a strain of B. cinerea that synthesized an acid proteinase. 



Aliphatic compounds 

B. cinerea was shown by Kosuge and Dutra (1962, 1963) to fix carbon 
dioxide during germination, i^c appeared mostly in amino and other organic 
acids when supplied in the medium as Na2i4C03. 

Species of Botrytis are able to form citric acid in a wort agar containing 
calcium carbonate and to deposit calcium citrate (van Beyma 1930; Schreyer 
1931; Behr 1968, 1969). Pollettini (1961) demonstrated the enhanced growth 
of B. cinerea in Raulin's solution with 2.5% and 11% lactic acid both in 
normal and oxygen-depleted atmospheres. 

B. cinerea is able to utilize citric and oxalic acids very poorly (Stalder 
1954) and pyruvic, acetic, and proprionic acids not at all. It is able to utilize 
malic and tartaric acids (see Part 4, "Enology"). Novak and Voros-Felkai 
(1958) found that B. cinerea^ utilized several aliphatic acids (lactic, citric, 
tartaric, succinic, fumaric, malonic, and ascorbic), as well as sodium lactate, 
sodium acetate, and ethanol, but it could not utilize formic, proprionic, oxalic, 
or acetic acids, nor sodium oxalate. With the exception of malonic acid, the 
data supported the hypothesis of a Krebs cycle, but Novak (1958) was able 
to reconcile this apparent departure. He found that malonate is decarboxylated 
to acetate and oxidized to succinic and oxalic acids. At a concentration of 
0.005 M or less, malonic acid stimulated oxygen consumption and there was 
no succinodehydrogenase activity, so that sugars were probably directly 
oxidized. 

Gluconic acid is not synthesized from sucrose by B. cinerea (Schreyer 
1931). 

Of probable significance in predisposition to infection (q.v.) is the 
ability of a Botrytis sp., reported as B. spectabilis (Hag and Curtis 1968), to 
form ethylene from simple media. A culture produced 0.25 ppm in 24 h, a 
concentration known to predispose certain tissues to attack by B. cinerea. 

Botrytis cinerea has been reported to oxidize straight-chain primary 
alcohols (except methanol), aromatic alcohols, and unsaturated primary al- 
cohols to yield the corresponding aldehydes and an equal molar quantity of 
H2O2 (Fukuda and Brannon 1971). The introduction of a polar group into 
the alcohols completely inhibited oxidation. 

50 



Vitamins 

According to Lilly and Barnett (1949) and Gough and Lilly (1956) 
B. cinerea apparently needs no exogenous source of vitamins; they found that 
it grew as fast in a simple medium as in one augmented with thiamine, biotin, 
inositol, or pyridoxine. On the other hand, Singh (1940) had found that 
conidial germination was enhanced by the addition of a lentil extract that 
contained thiamine, biotin, and perhaps other growth factors, and Olivier, 
Akhavan, and Bondoux (1972) found that B. cinerea grew better in the pres- 
ence of biotin, together with DL-trytophan and glycine. 



Trace elements 

Of minor elements, Metz (1930) considered zinc to be essential for the 
growth of a Botrytis sp. and, to a lesser extent, copper and iron; all were 
necessary for normal coloration. Young and Bennett (1922) found no marked 
effect of zinc in the nutrition of B. cinerea, but Valaskova (1963«) found it 
to limit growth without affecting sporulation or sclerotial formation in B. 
tulipae. Molybdenum in trace amounts enhanced the growth of B. cinerea 
(Castiglione and Landi 1948), but calcium had little effect on B. allii (Young 
and Bennett 1922). Trace elements in approximately the concentrations found 
in grape juice stimulated the formation of sclerotia by B. cinerea (Vanev 
1966); the trace elements were iron, zinc, boron, calcium, potassium, copper, 
phosphorus, manganese, and molybdenum. 

Cultures of B. gladiolorum did not grow or color normally in the ab- 
sence of magnesium and zinc (Marshall 1955), and sporulation was depressed 
in the absence of iron. 

Sulfur can be utilized by B. cinerea in the form of sulfate, persulfate, 
sulfite, or sulfhydryl (Armstrong 1921). B. cinerea is, however, very sensitive 
to sulfur dioxide (Couey and Uota 1961) acting as sulfurous acid. Sodium 
fluoride significantly suppressed the growth of B. cinerea at 5 X 10"3 M 
but at lower concentrations (e.g., 10"4 M and 10"5 M), growth was stimulated. 
Sporulation was abundant at the lower concentrations; even at 5 X 10"^ M 
there were a few conidiophores, but fewer at 10 2 M. Sclerotia were highly 
variable in number, but their viability was unimpaired at concentrations 
below 5 X 10-2 M (Treshow 1965). 



Alkaloids 

Botrytis cinerea tolerates and utilizes 2% caffeine and quinine (Ravaz 
and Gouirand 1896); 2% tannin, 2% amygdalin, 1% brucin, and 1% 
strychnine (though not of 20% quinine orthein, Biisgen 1918); 2.5% nicotine 
and 1% aconitin (but some inhibition by 2% atropine sulfate and slight 
inhibition by 4% quinine sulfate, Nobecourt 1921); and 2% atropine sulfate, 

51 



4% quinine sulfate, and 2.5% nicotine (Fischer and Gaumann 1929). Blu- 
mer and Gondek (1946) studied the action of oxyquinolins on B. cinerea. 
The alkaloids tomatin and solanin were found by Kern (1952) to have LD50 
values of 2 X 10 ^ M for germinating conidia of B. allii (B. aclada). 



Pigment production 

Several v^orkers, for example, Sprague and Heald (1926), Morquer 
(1933), Peyronel (1934), and Ellerbrook and Lorbeer (1972), have noted that 
some isolates of B. cinerea produce a red pigment in culture, but its identity 
and mode of production are not known. 



Hydrolytic enzymes 

The intracellular localization of some hydrolytic enzymes has been 
studied by Pitt and Walker (1967) and Pitt (1968, 1969). In cytoplasmic 
particles, Pitt found a latent acid phosphatase, carboxylic esterase, acid 
deoxyribonuclease, ^-galactosidase, and some suggestion of aryl sulfatase 
and peroxisomes. He found no ^-D-glucuronidase. 

Tseng and Bateman (1968) and Tseng, Lee, and Chang (1970) found 
that B. cinerea produced an extracellular phosphatidase in culture that re- 
leased palmitic acid, linoleic acid, and glycerylphosphorylcholine from soy- 
bean lecithin. This phosphatidase was also detected in parasitized onion. 

Pollettini (1962) investigated alkaline phosphatase activity in B. cinerea 
in relation to exposure to X-rays. Check cultures had a steadily decreasing 
enzyme activity; irradiated cultures had enhanced activity up to the 5th day 
and thereafter activity decreased and was undetectable by the 8th day. 

Hislop (1957) investigated the effect of some fungicides on enzymes of 
B. cinerea. Copper sulfate depressed catalase and increased cytochrome-C- 
oxidase activity; 0.05% stimulated peroxidase activity threefold but 0.1% 
depressed activity by 95%; captan enhanced catalase and cytochrome-C- 
oxidase but depressed peroxidase activity; o-phenylphenol increased cyto- 
chrome-C-oxidase and alkaline phosphatase, and depressed catalase and 
peroxidase activity; lime sulfur depressed all enzyme activity. 



Polyphenols 

Dubernet and Ribereau-Gayon (1973) concluded that the polyphenol 
oxidase of Botrytis cinerea is a laccase, which degrades the anthocyanins of 
grape berries as well as tannins (leucoanthocyanins) and several other phe- 
nolic substances such as pyrocatechol, phloroglucinol, p-cresol, gallic acid, 
DOPA, vanillic acid, caffeic acid, ferulic acid, chlorogenic acid, and ^-catechin. 

52 



This activity contrasts with the tyrosinase activity of the grape berry (see 
PART 4, "Enology"). 

Scurti, Fiussello, and Jodice (1972) considered that B. cinerea could 
utilize lignin, lignosulfonate, and humic and fulvic acids in litter decom- 
position. 

Botrytis allii (B. aclada) produces a complex phenolic compound, botral- 
lin, probably by the oxidative conversion of a substituted resorcinol ring into 
catechol or pyrogallol derivatives (Kameda, Aoki, Namiki, and Overeem 
1974). 



Test organisms 

Botrytis species are common test organisms for a wide variety of fungi- 
cides, pesticides, growth substances, antibiotics, etc. In general, in vitro and 
in vivo tests give similar indications, although there are anomalous results, 
which may, in part, be interpreted in terms of altered host-susceptibility (q.v.). 
Brook (1957) found general agreement between the two types of test, except 
in the case of copper; conidia of B. cinerea germinated on heavy deposits of 
copper on glass or cellulose nitrate surfaces in the absence of free water, but 
not in aqueous suspension. Copper compounds were ineffective in controlling 
the fungus on tomato plants, though LD50 values were lower than those of 
nearly all other materials tested. 

Chancogne and Fruchard (1965), Chancogne and Lefumeux (1967), and 
Lafon and Boniface (1971) found fungicides to act differently against conidia 
and mycelium of B. cinerea. 

B. cinerea is able to induce antibody formation in rabbits, and Preece 
and Cooper (1969) prepared a specific test reagent for the fungus from rabbit 
7 -globulin labelled with fluorescein isothiocyanate. The fungus could also be 
stained if treated with antiserum conjugated with a dye and then stained with 
a commercial goat antiglobulin conjugated with fluorescein isothiocyanate. 



SURVIVAL 



Although sclerotia are regarded as the fungal structures best adapted to 
withstand adverse conditions, surprisingly few detailed studies on their sur- 
vival have been made within the genus Botrytis (Willetts 1971). 

Townsend (1952) found that sclerotia of B. cinerea were killed within 
3 days when held at 80°C; the LD50 time at 66°C was 9 days and only 10% 
were viable after 13 days and none after 18 days. Survival was a little better 
at 54°C, while at 4°C, 100% survived for 81 days and 50% for 103 days; 

53 



all were dead after 123 days. At 20-25°C, sclerotia were still viable after 
5 mo. The loss in viability, particularly at high temperatures, did not seem to 
be the result of desiccation. In soil with a 35% moisture content, no sclerotia 
survived for more than 1 mo, but survival was better in dryer soil; all survived 
in soil of 17% and 8% moisture content for more than 8 mo. Submersion in 
water for 30 wk did not impair viability. Similar results were obtained by 
Kochenko(1972). 

Little is known of the survival of Botrytis spp. in field soil. Jeffries and 
Hemming (1953) found soil water to be fungistatic to B. allii (B. aclada) and 
Park (1955) and Lockwood (1960) noted that conidia of B. cinerea disap- 
peared quickly when put into soil and the fungus did not colonize pieces of 
plant material below the surface. However, the fungus survived 4 wk on 
previously colonized pieces of clover stem and 2 wk on grass. Hsu and 
Lockwood (1971) considered B. cinerea to be only a moderate competitor 
in soil. Fungistasis of B. cinerea by Trichoderma koningi in soil is probably 
pH-dependent (Schiiepp and Frei 1969). Park (1954) obtained chlamydo- 
spores of B. cinerea in soil solutions but their survival in soils seems not to 
have been evaluated. 

Although the main structures adapted to survival in Botrytis spp. are 
the sclerotia and occasionally the chlamydospores (q.v.), conidia are also 
able to survive in normal field conditions quite well (Ilieva 1970; Vyskarko 
and Vaselashki 1973), although van der Spek (1960) found that the viability 
of conidia of B. cinerea decreased with age and Doran (1922) noted that 
young conidia germinate over a wider range of adverse conditions than older 
ones. Last (1960^) found the same viability in conidia of B. fabae. Hennebert 
and Gilles (1958) found that the decline in viability of conidia at a relative 
humidity of 60-70% and 15-20°C is accelerated by direct insolation. After 
a 3-day exposure, including one 3-h insolation period, only 3-5% of conidia 
germinated, and none were viable at the end of 10 days. Air-dry conidia, 
95% of which were viable, were exposed in the shade; after 1 day 20% were 
still viable, after 3 days 11%, and after 12 days 5% . 

Ultraviolet light can be rapidly fungicidal to Botrytis spp. (English and 
Gerhardt 1946; Masago 1959). Spores of a Botrytis sp. from apple were 
killed on the surface of agar by a 1-min exposure to an ultraviolet light source 
15 cm away (Fulton and Coblentz 1929). Savulescu and Tudosescu (1968) 
found B. cinerea to be one of the most sensitive fungi they tested, although a 
single exposure of 15-30 min stimulated mycelial growth. Exposures of 
longer than 2 h decreased viability, as was also found by Chebotarev,Lanetskii, 
and Nabarezhnyk (1968). Ultraviolet light also reduced the ability of B. fabae 
to initiate colonies on agar (Buxton, Last, and Nour 1957), but damage to 
the conidia was partially reversed by subsequent exposure to daylight. The 
reason for this is unknown. 

When conidia of B. cinerea were allowed to germinate, dried for 8-12 h, 
remoistened, redried, and allowed to grow on, 60-90% of them survived 
(Good and Zathureczky 1967). The proportion surviving decreased only 

54 



slightly with increasing germ tube length. Losses from the second drying were 
only slightly higher than from the first. 

On living tomato leaves, conidia of B. cinerea remained viable for 3 mo 
and for 10-16 mo when the leaves were stored dry in the laboratory (Ilieva 
1970). 

Jarvis (unpublished) kept conidia of B, cinerea submerged in water of 
depths ranging from 9 to 36 mm and at temperatures between 10°C and 
30 °C. When the conidia were removed from the water 2 days after submer- 
sion, 10-40% germinated; when removed after 11 days, 1-10% germinated. 
Fewer germinated after submersion at 10°C and 30° C than at 15°C or 20°C, 
and a much higher proportion of conidia germinated when they were recov- 
ered in clumps. Occasional conidia germinated after submersion for 25 days. 
The depth of water, in which the conidia sank to the bottom, had no effect 
on survival. 

Conidia of B. tulipae were found by Beaumont, Dillon Weston, and 
Wallace (1936) to be viable for 1-50 days and some for 6 mo when stored 
dry in the laboratory. They thought sclerotia would be viable for at least 2 yr. 

Maas (1969) found that survival of conidia and sclerotia of B. convoluta 
was favored by low temperatures; storage at — 70°C only sUghtly impaired 
germinability of conidia after 257 days and of sclerotia after 366 days. Expo- 
sure to 30 °C, however, rapidly decreased the viabiUty of conidia, and sclerotia 
held at 30°C for a year lost 65% of their germinability. Sclerotia held in 
moist, non-sterile soil at temperatures higher than 15°C rapidly lost their 
germinability, probably, it was suggested, because of antagonism and para- 
sitism by other organisms. 

Botrytis spp. are able to live well and parasitize plants at relatively low 
temperatures (see also PART 4, "Resistance"). For example, Sato, Shoji, and 
Ota (1959) found a Botrytis of the cinerea type causing a snow mold of conifer 
seedlings; viability of the pathogen was unimpaired by several days' exposure 
to — 7°C. B. cinerea can be pathogenic at temperatures around 3°C, but 
Vanev (1965) noted that temperatures fluctuating around 0°C rapidly killed 
conidia. Bartetsko (1910) found that conidia of a Botrytis sp. were viable after 
immersion in a liquid medium at — 14°C for 2 h. Young mycelium survived 
better if it was frozen in a 5% glucose solution than in a 1% solution, and 
Purvis and Barnett (1952) successfully preserved conidia of B. cinerea in a 
frozen aqueous suspension for 2 yr. 

Van den Berg and Lentz (1968) found that the mycelium of B. cinerea 
can survive under the usual conditions of storage for vegetables. In the 
absence of nutrients, the myceUum survived at 0°C more than 12 mo in a 
saturated atmosphere, and 2-12 mo in a relative humidity of 85%; at 20°C 
the mycelium survived 5-12 mo, and less than 1-5 mo in the respective 
relative humidities. When the mycelium was supplied with nutrients, no 
growth occurred in relative humidities below 93% and the mycelium survived 
less than 1 month. Conidia at 0°C survived 3-6 mo in 99% RH and 2-6 mo 

55 



at 85%; at 20°C conidia survived less than 1-3 mo and less than 1 mo at 
the respective RH. 

Bulit, Bugaret, and Verdu (1973) failed to detect B. cinerea in the buds 
of the grapevine after winter in the field in Bordeaux. 

In a high temperature study, O'Brien (1902) found that 5- and 10-min 
exposures to 50°C resulted in 65% and 2% germination of conidia of B. 
cinerea respectively; and exposure to 53 °C was lethal. 

In a study of soil pasteurization, Zumstein (1935) found that for B. 
cinerea the minimum lethal high temperature, maintained for 15 min, was 
55°C. Vanev (1965) found that some conidia of B. cinerea survived a 2-min 
exposure to 170°C, but Ogawa and McCain (1960) killed dry conidia on 
glass rods by a 1-sec exposure to live steam. 

The susceptibility of B. cinerea to heat has been used as the basis of 
pasteurization treatments to control gray mold in strawberries (Smith and 
Worthington 1965; Couey and Follstad 1966). Fruit decay was considerably 
reduced by exposures of 20 or 30 min at 44°C and 98% RH or 60 min at 
90% RH; lower humidities were not effective. Raspberries were less success- 
fully treated (Worthington and Smith 1965); although decay was retarded, 
heat injury to the fruit was unacceptable. These treatments are unlikely to 
be of commercial value because of the fine degree of temperature control 
required. 

Smith (1923Z)), exposing conidia of B. cinerea in water for 3 h at 37 °C, 
found that subsequent germination on Czapek agar was delayed; after a 24-h 
incubation, 49.8% germinated and after 48 h, 74.4%. Shorter exposures did 
not result in a delay in germination, and Smith suggested that killing is a 
gradual process and that 'half dead' conidia may recover on prolonged incuba- 
tion. Smith produced several curves showing the effects of high temperatures 
on conidia and introduced the concept of LD50 values, the exposure time 
when half the conidia were killed. The curve log LD^q time - 1/T° was a 
straight line, and the effect of temperature on the killing reaction velocity 
was unusually great. 

Smith (1921) also made a study of the response of conidia of B. cinerea 
to phenol. A plot of the percentage of conidia surviving against exposure time 
gave a sigmoid curve and a plot against phenol dose gave a logarithmic curve. 
A higher concentration of conidia had an effect equivalent to reducing phenol 
concentration or to using very young conidia. Smith (1921) considered that 
the killing of conidia by phenol involves 2 processes, penetration and then 
the action of phenol on metabolic processes. 

Blumer and Gondek (1946) made a similar study of the action of oxy- 
quinolins on B. cinerea and McCallan and Weedon (1940) one on the action 
of SO2, HCN, H2S, CI 2, and ammonia. 

The conidia and mycelium of B. cinerea are killed by gamma radiation 
(Terui and Harada 1964; Barkai-Golan, Temkin-Gorodeiski, and Kahan 

56 



1967). Mycelium irradiated by 80 X 10^ rad at a rate of lO^^ rad/h was 
almost completely killed, but that irradiated at 2 X 10-* rad/h was capable 
of renewed growth; the rate of irradiation, as well as the dose, is therefore 
important. Growth, sporulation, and sclerotial formation in B. cinerea were 
reduced by 5-40 X 10^ rad. Established infections in grapes, especially old 
infections, were less susceptible to radiation than conidia were (Couey and 
Bramlage 1965). Sommer, Fortlage, Buckley, and Maxie (1972) demonstrated 
that conidia, mycelia, and sclerotia of B. cinerea had different sensitivities to 
gamma radiation, and Georgopoulos, Macris, and Georgiadou (1966) found 
that iodoacetamide at 70-100 ppm considerably enhanced the effects of very 
low radiation doses (4 krad) in conidia of B. cinerea. 

Irradiation of fruits and vegetables has been tried often as a postharvest 
control measure, but the gamma radiation dosages, except on strawberries 
and radishes, are detrimental to quality (Eckert and Sommer 1967). 

Metlitsky and Soboleva (1936) and Tverskoy (1937) found that irradia- 
tion at wavelengths of 5-40 m killed B. cinerea in culture. 



DISPERSAL 



All 5o/ry//5 spp. sporulate profusely; in most species the dry conidia are 
dispersed through the air in large numbers on air currents and thus these 
species fall into the anemochoric group of plant pathogens of Stepanov 
(1935). Nutrient agars in petri dishes exposed from aircraft have revealed 
the presence of Botrytis spp. in the air over the Arctic and Atlantic Oceans 
(Pady 1951; Bisby 1935; and Pady and Kelly 1954). At lower altitudes, 
conidia have been recorded in urban areas (Pady and Kapica 1956), mainly 
in the summer (Pawsey and Heath 1964) and autumn (Hyde and Williams 
1949). Richards (1956) found them more abundant in rural areas where they 
comprised 2.2% of all spores trapped, but Gregory and Hirst (1957), using 
an automatic volumetric spore trap, found that they comprised only 0.42% 
of spores trapped at Rothamsted over the summer of 1952, with a peak in 
June of 288/m3 of air sampled. Sreeramulu (1959), also at Rothamsted, 
found a diurnal periodicity with a peak of about 400/m3 at midday. Spores 
began to appear in June and reached a peak between June 22 and July 2. 
Lacey (1962) found peaks of about 1500 conidia/m^ and a mean concentra- 
tion for a summer season of 1.2% and 1.6% of the total conidia trapped at 
two rural sites. Kimura and Yamamoto (1972) investigated the concentration 
oiB. cinerea in the air spora in Japan, and Cejp (1947) in Czechoslovakia. 

Matsuo et al. (1973) investigated the dispersal of conidia of B. allii 
(B. aclada) in onion packinghouses. 

The mechanism of spore dispersal is best known in B. cinerea, having 
been first described by de Bary (1884); and Hopkins (1921) first described 

57 



the mechanism in B. tulipae. According to them, the mature conidiophore is a 
flattened, twisted ribbon; it responds to changes in the relative humidity of 
its environment by twisting about its long axis sufficiently violently to fling off 
the spores by centrifugal force, an observation which Ingold (1939) could 
not confirm. 

Jarvis (1960/?), using an apparatus to transfer sporulating cultures of B. 
cinerea between environments of differing relative humidity without mechan- 
ical shock or exposure of the cultures to an external environment, found that 
the conidiophore is as de Bary described, and though it twists about its long 
axis, the movement is not violent. In a profusely sporing culture, the ampullae 
and conidia of adjacent conidiophores are tangled together. The hygroscopic 
movements gently but jerkily dislodge the conidia from their fine attachment 
to the ampullae among which they come to lie loosely and whence, in the 
open laboratory or field, they may be readily dispersed on air currents or by 
other agencies. 

Thus, Jarvis (1962/?) distinguished two processes in spore dispersal; 
first the hygroscopic mechanism of spore release, followed by true dispersal 
by other agencies. 

These two processes probably occur in other species, for example, in 
B. tulipae (Hopkins 1921), but no detailed examination has been made. 
Mason (1937) considered spore release in B. cinerea to be brought about by 
the withering of the sterigma connecting spore and ampulla at maturity. 

Of particular speculative interest are those species (e.g., B. squamosa 
and B. glohosa) in which the conidiophore twists in response to desiccation, 
its branches contract, and after spore release, the ampullae suddenly collapse 
in conspicuous accordion-like folds (Viennot-Bourgin 1953; Webster and 
Jarvis 1951; and Hennebert 1963, 1973). This rapid collapse suggests some 
release of internal pressure; however, no explosive discharge of conidia of the 
type occurring in, for example, Pilobolus spp. has been recorded. The conid- 
iophore of B. squamosa can regain turgidity after spore release and form 
new spores laterally and terminally. 

Mature conidiophores of B. cinerea contain a variety of cytoplasmic 
arrangements, including hollow reticulate cylinders, spiral arrangements, and 
structures resembling internal hyphae, which themselves may be flattened and 
twisted, and it may be speculated that uneven distribution of cytoplasm may 
account, in part, for hygroscopic movements (Jarvis, unpublished). 

The positive phototropism of the conidiophore (q.v.; Jarvis 1972) is 
likely of significance in spore dispersal, although its role in the field has not 
been assessed. 

Spore liberation by Botryds cinerea from necrotic leaves of Chrysan- 
themum morifolium and Allium cepa was investigated in controlled environ- 
ments by McCoy and Dimock (1971). At 20°C, spore release was condi- 
tioned by the presence of free moisture in the substrate, by the degree of 
atmospheric turbulence, and by mean wind velocity, although the effect of 

58 



the last was secondary because release did not occur in the absence of free 
moisture. Over 98% of conidia trapped were released in 2 daily periods of 
5 h each. McCoy and Dimock suggested that the liberation of conidia depends 
on free water in the substrate and that the effect of wind is primarily on 
dispersal. Stepanov (1935) considered that the minimum wind speed necessary 
to disperse conidia of B. cinerea was about 0.36-0.50 m/s, and that conidia 
could even fall oif under gravity. The terminal velocity was calculated to be 
0.22-0.45 cm/s by Gregory and Denton (Gregory 1973). Stepanov found 
dispersal in convection currents. Hamilton (1957, in Gregory 1973) found 
that the dispersal of Botrytis conidia decreased significantly with increasing 
wind speed. 

The patterns of spore dispersal of B. cinerea in Scottish raspberry and 
strawberry plantations were examined by Jarvis (19626, 1962c) using an 
automatic volumetric spore trap. In raspberry plantations there is a basic 
diurnal pattern of two periods of prolific spore dispersal corresponding to two 
periods of rapidly changing relative humidity. The first, from midmorning 
until about noon, is typically a period of drying of dew when the relative 
humidity falls rapidly from about 85% to 65%; conversely, the second is an 
evening rise in relative humidity between the same approximate limits as dew 
is formed again. Thus, the field conditions reflect those of the laboratory 
(Jarvis 19606) when spore release was achieved by both rising and falling 
changes in relative humidity of as little as 5% . 

The stylized pattern can, of course, be considerable modified by other 
climatic factors. Jarvis (19626) found that conidia were not generally dis- 
persed unless the temperature of the preceding night was at least about 12°C 
and deduced that this was the minimum temperature for mature spore pro- 
duction. As many as 2 X 10^ spores/ms of air were recorded at a height of 
1 m during the morning dispersal period and the spores remaining undis- 
persed then contributed, in suitable conditions, to the air spora of the after- 
noon period. The relatively small humidity changes induced by intermittent 
sunshine often produced moderate spore concentrations throughout the day. 

More striking were the relatively high concentrations of airborne spores 
associated with rain showers, often in conditions otherwise unsuitable for 
dispersal (Lacey 1962; Jarvis 19626). As had been observed in the laboratory 
(Jarvis 1960), the mechanical shock of raindrops falling onto conidiophores or 
near their substratum could cause jerky disentanglement of conidiophores and 
ampullae, so that spores were released to be dispersed on the shock air waves 
and other air currents. Perhaps changes in relative humidity in the vicinity of 
impacting raindrops also operate the hygroscopic mechanism. Dillon Weston 
and Taylor (1948) found that a single water drop falling onto a Botrytis- 
infected leaf could contaminate an area of some 2,5 m^ with spores; if the 
leaf was exposed to a rain shower lasting 45 min, the contaminated area 
was more than 32 m2. In one splash droplet, 156 conidia were counted. 

Investigating further the role of rain in spore dispersal, Jarvis {\962d) 
found that water dropped onto a sporulating culture of B. cinerea in the 

59 



laboratory produced splash droplets completely coated with dry spores. These 
projectiles, travelling for distances up to about Im, were remarkably stable 
and could be manipulated with forceps until the water within began to evapo- 
rate. The projectiles then invaginated and finally collapsed. However, if water 
did not evaporate quickly in the field, it is possible that spores would eventu- 
ally become wet enough to enter the drop and begin germination. The role 
of these projectiles in epidemiology has not been investigated. 

Hislop (1969) obtained infection of leaves of Vicia faba from rain- 
splashed conidia of Botrytis fabae and observed that they could be splashed 
to the underside of leaves. Beaumont, Dillon Weston, and Wallace (1936) and 
Price (1967) noted dispersal by rain in B. tuUpae and Beaumont et al. further 
noted that this type of dispersal could also occur in greenhouses when con- 
densate dripped from the roof. Corbaz (1972) also found rain to be important 
in the dispersal of spores of B. cinerea in the vineyard and, unlike Jarvis 
(19626), considered disturbance of infected berries by pickers to be an im- 
portant factor. In many aspects, the patterns of dispersal in a vineyard and a 
raspberry plantation are very similar (Jarvis 19626; Bulit and Lafon 1970; 
Corbaz 1972; and Bulit and Verdu 1974). 

In raspberries and in grapes, the sporulating sites of sclerotia of B. 
cinerea are mostly well above the ground on stems, on diseased berries, and, 
in raspberry, on receptacles remaining after the drupelets are picked, and so 
all are well-exposed to the changing environment. In strawberry plantations, 
however, the sporulating sites — diseased berries and colonized debris — are 
not so exposed; trapping at a height of 0.5 m, just above the leaf canopy, 
showed that very few spores become airborne in the same conditions dis- 
persing spores in nearby raspberry plantations (Miller and Waggoner 1957; 
Jarvis 1962c). Only on days when picking occurred did appreciable spore 
concentrations occur in the air over the strawberry plantation, and then the 
concentrations were closely correlated with the numbers of affected berries 
beneath the canopy (Jarvis 1962c). The disturbance of the leaves, of necessity 
on dry days, changed the relative humidity around the sporulating sites, 
permitting dispersal. Undisturbed, sporulating sites have a microclimate that 
is continually near-saturated, and no hygroscopic movements occur; air cur- 
rents are also minimal. By contrast. Miller and Waggoner (1957) trapped 
most spores in conditions of high relative humidity. 

In onion crops, Lorbeer (1966) noted a diurnal periodicity of conidia of 
B. squamosa; 80% were collected between 8 a.m. and 4 p.m. He related peak 
concentrations to increases in temperature rather than to changes in relative 
humidity, and found that the same pattern of diurnal periodicity occurred in 
a 36-h period of relative humidity continuously at 97% . 

Saprophytically based inocula of B. cinerea may be very important in 
the epidemiology of the gray mold diseases (Jarvis 1962«), and wind-blown 
and rain-splashed pieces of colonized debris are probably effective dispersal 
propagules as in Whetzelinia sclerotiorum and Sclerotinia minor (Natti 1971; 
Jarvis and Hawthorne 1972; and Hawthorne and Hartill, personal commu- 

60 



nication). Maas and Powelson (1970) also pointed out the importance of 
symptomless, latent infections in the survival and dispersal of Botrytis con- 
voluta in rhizomes of Iris; other latent infections (q.v.) probably can have 
similar roles. 

Although the conditions for maximum airborne spore dispersal can be 
approximately defined, at least in crops like raspberry and onion, the knowl- 
edge is of little value in forecasting epidemics. Of much more value is a 
knowledge of the conditions for successful infection and even then spores 
may play a relatively minor part, as in raspberry and strawberry (Jarvis 
\962d). 

Many species of Botrytis are seed-borne, especially in the sense that 
sclerotia are mixed with seed, although some, for example, B. tulipae, are 
carried as mycelium within the seed (Capelletti 1931). Noble and Richardson 
(1968) list (with bibliography) the following: Botryotinia ricini, B. theae, B. 
porri, B. squamosa, Botrytis allii, B. anthophila, B. byssoidea, B. fabae, 
Botrytis sp. (including B. parasitica = B. tulipae) on 3 hosts, and B. cinerea 
on 44 hosts. Dispersal may thus take place with seed dispersal, including that 
of commerce and by other agents that disperse seeds (for example, birds and 
rodents). 

In the specialized species B. anthophila (sporulating on the anthers of 
clover), bees and other insects probably disperse the sticky spores (Silow 
1933). Bees also dispersed the spores of B. cinerea in a strawberry plantation 
(Kovacs 1969). Of two pests of tomato glasshouses, Drosophila melanogaster 
was found only rarely to carry the spores of B. cinerea (Butler and Bracker 
1963), but Aleyrodes vaporariorum did carry those of a Botrytis sp. (Dickson 
1920). Ondrej (1973) found that in Czechoslovakia spores of B. fabae were 
carried by the thrips Acyrthosiphon onobrychis but not by Aphis fabae or 
Thysanoptera, and that flower infestation by B. fabae could be reduced by 
insecticides. Spores of B. gladiolorum were found to be dispersed by a mite, 
Pediculopsis sp. that was apparently an obligate symbiont of the fungus 
(Harrison 1952). 

The mechanisms of ascospore discharge and dispersal in Botryotinia 
spp. are largely unknown. There is explosive discharge from apothecia of 
B. ricini (Godfrey 1923), which is apparently similar to the puffing phenom- 
enon in Whetzelinia (Sclerotinia) sclerotiorum (Dickson and Fisher 1923; 
Buller 1934) and probably triggered by a hygroscopic response. Frequently 
the 8 spores are dispersed together. The stipe, and possibly the asci, of B. 
ricini (Godfrey 1923) and of B. fuckeliana (Gettkandt 1954) show positive 
phototropism that may be of phytopathologic significance. 



61 



PART 4 PATHOLOGY 



HOST SPECIFICITY 



Some Botrytis species, previously believed to be host specific and hence 
often given the host name in the specific epithet, are now known to have a 
somewhat wider host range. Thus, Botrytis tulipae occurs not only on Tulipa, 
but also on Lilium regale (Hennebert 1971); fi. gladiolorum is probably patho- 
genic to Crocus versicolor; and Botrytis elliptica, formerly recorded only on 
Lilium spp., also occurs on Colchicum autumnale, Gladiolus spp., Erythro- 
nium grandiflorum var. pallidum, Polyanthus tuberosa (MacLean 1948; Mac- 
Lean and Shaw 1949; and Ark and MacLean 1951), Stephanotis floribunda, 
and, by inoculation. Cyclamen indicum (Tompkins and Hansen 1950). 

In general, fairly close host-specificity occurs in Botrytis spp. on the 
corolliferous monocotyledons and the Ranunculaceae (Hennebert 1963; Hen- 
nebert and Groves 1963; Hellmers 1943; Moore 1954; Yamamoto, Oyasu, 
and Iwasaki 1956; Kovachevski 1958; and Nieuwhof and Meer 1970). For 
example, Botrytis spp. occurring on Allium spp. (Hennebert 1963) are: 

A. ascalonicum B. aclada (B. allii), B. cinerea, (B. porri by inocu- 

lation) 

A. cepa B. aclada, B. byssoidea, B. cinerea, B. squamosa, 

{B. globosa, B. porri by inoculation) 

A. fistulosum B. aclada, B. byssoidea 

A. porrum B. aclada, B. byssoidea, B. cinerea, B. porri 

A. sativum B. aclada, B. byssoidea, B. porri 

A. schoenoprasum B. aclada, B. byssoidea 

A. triquetum B. sphaerosperma 

A. ursinum B. globosa 

A. vineale B. porri 

Thus, close host-specificity occurs only in B. sphaerosperma and possibly B. 
globosa in the wild, and outside the 2 groups mentioned above, host speci- 
ficity is probably exclusive only in B. spermophila, B. anthophila, and B. 
pelargonii. 

Though bearing a host name, B. fabae is not host specific; it occurs not 
only on Vicia faba, its first described host (Sardina 1929), but also on V. 
cracca, V. sativa. Lens culinaris, Pisum sativum, P. sativum var. arvense, and 
Phaseolus vulgaris, though all in the Leguminosae (Sardina 1931; Yu 1945). 

B. fabae is often confused with B. cinerea on beans (Wilson 1937; Ogilvie 
and Munro 1947); of 168 isolates from V. faba grown in various parts of the 

62 



USSR, 152 were ascribed to B. jabae and 16 to B. cinerea by Vasin and 
Gorlenko (1966^, 1966/?). They found B. fabae to be variable in culture, 
with conidial size sometimes approaching that of B. cinerea, and they recorded 
B. fabae as a form of B. cinerea adapted to bean, but now sufficiently distinct 
to warrant species rank. Sundheim (1973) clearly distinguished them in Nor- 
way, as did Ondrej (1973) in Czechoslovakia and Shidla (1973) in Lithuania. 

Sometimes, supposed host-specificity has been reflected in the erection 
of a forma specialis within a species, usually with confusion (Westerdijk 
1927). For example, Hodosy (1964) erected B. cinerea f.sp. convallariae, 
which however more resembled B. tulipae, although Klebahn (1930) had 
accepted B. convallariae as a good species, as did Hennebert (1971). Klebahn 
(1930) erected four formae speciales within B. cinerea distinguished by spore 
size rather than by the results of pathogenicity tests: f.sp. primulae from 
Primula (with conidia measuring 10.5 X 6.3 /xm), f.sp. prunitrilobae (9.2 X 
5 /xm), f.sp. syringae from Syringa vulgaris (12.6 X 8.3 fxm), and f.sp. vitis 
from Vitis vinifera (12.6 X 6.8 /^m). Klebahn also distinguished B. parasitica 
and B. douglasii on biological grounds, but referred both to B. cinerea on 
morphological grounds. Van Beyma (1930) added another forma specialis 
of B. cinerea, f.sp. lini. Isolated from flax seed, it was considered to differ 
from B. cinerea in certain conidial and cultural characters. Another, B. 
cinerea f.sp. coffeae, was described by Hendrick (1939) from coffee fruits. 
He differentiated it on conidial size rather than on the results of pathogenicity 
tests, although he assumed it to be host specific. 

In the subtropical conditions of Georgia SSR, Hazaradze and Nisnianidze 
(1961) believed B. cinerea to be an aggregate species and, on slender evidence, 
they recognized as host specific the formae speciales citri-limon, citri-sinensis, 
citri-nobilis, diospyri, and aleurites. Though all ff.sp. were pathogenic to each 
host, ff.sp. diospyri and citri-limon were more so than the others. In culture, 
demarcation lines developed between colonies of the ff.sp. There were no 
significant differences in spore morphology or size. 

Kovachevski (1958) proved the pathogenicity of Botryotinia porri to 
garlic (Allium sativum), in addition to leek (A. porrum), in Bulgaria, but 
found onion (A. cepa) to be rarely infected. On these grounds, Kovachevski 
considered his fungus to be a new form, B. porri f.sp. allii-sativae. 

Differences in pathogenicity have been reported among isolates of 
Botrytis cinerea from lemon by Klotz, Calavan, and Zentmeyer (1946) and 
from grapevine by Fischer and Gaumann (1929), Pesante (1947), Kublitskaya 
and Ryabtseva (1969), and Kublitskaya, Ryabtseva and Vorob'eva (1970). 
Fischer and Gaumann (1929) noted greater pathogenicity in an isolate pre- 
dominantly forming mycelium in culture, but such an isolate may have 
greater inoculum potential in pathogenicity tests, so this report must be 
viewed with caution. A more pertinent observation is that of Kublitbskaya 
and Ryabtseva (1969) who found differential pathogenicity among isolates 
of B. cinerea to be directly correlated with the production of polygalactu- 
ronase. 

63 



Talieva (1958^) noted that species of Botrytis with a high degree of host 
specificity (e.g., B. aclada and B. anthophild) responded sharply in growth 
to autolysates from their hosts, whereas the polyphagous B. cinerea responded 
equally to autolysates from all hosts. Neither type responded to growth 
factors, referred to as 'bacterial vitamins'. 

An interesting and unusual case of pathogenic specialization in B. cinerea 
was noted by MacNeill (1953). A strain obtained from lettuce in the Bradford 
Marsh area of Ontario, Canada, was extremely pathogenic to the roots and 
caused deep furrows in them. The roots became coppery-green and eventually 
rotted completely. The strain rarely appeared on the foliage and then only 
after the plant collapsed. 

By contrast, Schnellhardt and Heald (1936) concluded that there was 
no host specificity among isolates of a Botrytis of the cinerea type isolated 
from apple, pear, pea, geranium, and Gloxinia and inoculated into apple 
fruits; and Peyer (1963) found no evidence of pathogenic races in isolates 
of B. cinerea from the stems and berries of grape; and Morotchkovski and 
Vitas (1939) found isolates of B. cinerea from sugar beet, soil, Pelargonium, 
rose, lemon, Primula, and Chrysanthemum to be equally pathogenic to stored 
sugar beet. 



INFECTION 



Infection from conidia 

The physical processes involved in host penetration by germ tubes of 
Botrytis cinerea have long been known. Ward (1888) described the infection 
of lily by germ tubes of a Botrytis sp. and Nordhausen (1899) investigated 
infection by B. cinerea. The process is best known, however, from the work 
of Brown and his colleagues, reviewed by Brown (1934, 1936, 1948, 1955) 
and, more recently, from the electron-microscope studies of Bessis (1972), 
Abu-Zinada, Cobb, and Boulter (1973), and McKeen (1974). 

Penetration of an intact host cuticle is purely mechanical according to 
Blackman and Welsford (1916) and Brown and Harvey (1927). The conid- 
ium, lying on the cuticle in a drop of water or nutrient solution, soon 
becomes attached to the substratum by means of an adhesive mucilaginous 
sheath investing the germ tube. Often penetration occurs directly from the 
distal end of the germ tube, but sometimes a typical digitate appressorium 
forms first, also invested by a mucilaginous sheath. In the area of contact 
between the germ tube tip, or appressorium, and the host cuticle, a small peg 
outgrowth penetrates the cuticle over a very small area (0.2 ^m in diameter; 
McKeen 1974), evidently by exerting mechanical pressure, because a small 
depression can often be seen below it. The tiipjel (pits), observed by Pfaff 
(1925) on appressoria of B. cinerea, have apparently not been reported since 

64 



and their function is unknown; perhaps they are artifacts and Pfaff misinter- 
preted infection pegs. 

McKeen (1974), reexamining the infection of leaves of Vicia faba by 
B. cinerea, differed from Brown and his colleagues; McKeen thought that the 
cuticle was dissolved enzymatically rather than pierced by mechanical pres- 
sure because the hole in the cuticle appeared to be sharp and clean without 
curled edges. Furthermore, McKeen could not see an indentation of the 
cuticle or epidermal wall during penetration, and he queried the early reports 
of penetration of undegradable materials such as gold film. 

Some support for McKeen's view is provided by Linskens and Haage 
(1963) who found that an isolate of B. cinerea could degrade potato leaf cutin 
and Gasteria leaf cutin. Shishiyama, Araki and Akai (1970) also reported a 
cutin-esterase from B. cinerea, which, they suggested, could reduce the me- 
chanical strength of the cuticle and so aid penetration. In the latter case, the 
enzyme was prepared from homogenates of mycelium growing in a medium 
containing tomato cutin as the sole carbon source. The enzyme hydrolyzed 
the minor fatty acids linked to the basic structure of cutin, but the major 
component, dihydroxyeicosanoic acid, did not appear in the hydrolysate. A 
preparation of tomato cutin had visibly, though slightly, degraded in struc- 
ture after prolonged incubation with the enzyme (30 days at 28 °C). Because 
the enzyme was not shown to be secreted in the infection drop and because 
of its apparent slowness of action, Shishiyama et al. thought that the enzyme 
played a very small part, if any, in infection, although it may play some part 
in saprophytic nutrition (Linskens and Haage 1963). Verhoeff (personal 
communication, 1973), however, obtained evidence from the infection of 
tomato fruit by B. cinerea that fungal cutinase probably plays a larger part 
in the penetration process than the results of Shishiyama et al. (1970) would 
suggest. 

After the bean-leaf cuticle was penetrated, McKeen found that the 
epidermal wall began to degrade and to split into two or more layers. The 
cuticle was pushed upwards, sometimes clear of the underlying and rapidly 
swelling epidermal wall. He detected esterase activity within the germ tube 
tip at the time of penetration and suggested esterases could aid in plasticizing 
the fungal wall and in dissolving the host cuticle. The small volume in which 
esterase activity could be detected histochemically could account for the 
failure of earlier workers to detect it by other means; also, activity soon dis- 
appears, within 23 h. At the time of penetration the infection peg is covered 
only by the fungal plasmalemma through which cutinase could pass readily. 

Abu-Zinada et al. (1973), working with B. fabae and V. faba, also con- 
cluded that penetration is probably accomplished by hydrolysis of the host 
cell-wall by fungal enzymes, although this stage is preceded by an attachment 
stage, with frequent invagination of the wall subsequently penetrated. There 
was no appressorium in the infection studied by Abu-Zinada et al. 

Louis (1963) agreed with Brown et al. on the penetration of bean leaves 
(V. faba) and tomato fruit. She showed that penetrations from a single germ- 

65 



tube of B. cinerea could induce a necrotic reaction in the neighboring host- 
cells in bean and tomato, but not in petals of Cyclamen and geranium or in 
leaves of Fuchsia. This behavior appeared to be related to cuticle thickness; 
the hosts with a thin cuticle had no necrotic reaction and were invaded by 
many germ tubes that formed confluent infections, whereas in bean and 
tomato, hosts with a thicker cuticle, the infections remained discrete. 

Often (for example, on almond petals, Ogawa and English 1960) the 
appressorium is formed at the junction of adjacent epidermal cells; when 
penetration is complete, the hypha widens beneath the cuticle and penetrates 
the remainder of the wall. 

In Lilium sp. (an edible lily), infection by germ tubes of Botrytis elliptica 
occurs directly through the leaf cuticle without the aid of wounding and 
spreads more rapidly on the lower than the upper surface because of the 
thicker cuticle and the absence of stomata on the upper surface (Ikata and 
Hitomi 1933). 

As well as penetrating the cuticle directly, germ tubes of B. cinerea 
are also able to penetrate stomata of bean (Vicia faba) and Dahlia leaves 
(Louis 1963), apple lenticels (Home 1932, 1933; Colhoun 1962) and all types 
of cracks and insect punctures in grape berries (for example, du Plessis 1937; 
Nelson 1951a; Stalder 1953^; Henner 1964; Bessis 1972; and Tonchev 1972), 
and in many other damaged tissues, such as those of tuberous rooted Begonia 
stems cracked by excessive nitrogen applications (Tompkins 1950) (see PART 
4, "Resistance" and "Predisposition"), Germ tubes of B. gladiolorum pene- 
trate stomata of leaves of Gladiolus when stomatal droplets are exuded in 
cool, moist conditions (Bald 1952). 

Using a scanning electron microscope, Bessis (1972) found that germ 
tubes of B. cinerea congregated above peristomatal tissues on grape berries, 
where there were minute cracks and fragments of disintegrated tissue. There 
was also a mucilaginous deposit in this region, apparently secreted by the 
host rather than the fungus. Penetration occurred in the peristomatal region 
but only rarely through the stoma itself. In effect, the fungus seemed to 
behave as a saprophyte on the surface of the peristomatal area before pene- 
trating beyond the cuticle. 

The stimulus for penetration was studied by Brown and Harvey (1927). 
Prior to this work, there had been considerable controversy about the factors 
affecting the direction of germ-tube growth, and a number of possibilities were 
considered and rejected by Brown and Harvey and in the reviews by Brown 
(1934, 1936). Positive chemotropism was first postulated by Miyoshi (1894, 
1895) but Fulton (1906) failed to confirm Miyoshi's results and suggested 
that germ tubes grow away from their own staling products in the infection 
drop. Graves (1916) found that some, but not all, plant extracts had a positive 
chemotropic effect on germ tubes, more so than sucrose, but he also supported 
Fulton's view. Miyoshi (1895), Lind (1898), and Brown and Harvey all found 
that penetration of non-plant membranes, such as paraffin wax and gold leaf, 
could occur in the absence of any apparent chemotropic stimulus, and Brown 

66 



and Harvey confirmed this with epidermal strips from Allium cepa bulb scales 
and leaves of Eucharis mastersi and E. amazonica, none having stomata. 
Penetration was achieved both in strips still with damaged cells attached to 
them, and in washed strips from which possible chemotropically stimulating 
cell contents had been removed. Penetration of washed strips occurred equally 
well in either direction. 

Brown and Harvey (1927) found that germ tubes of B. cinerea could 
not penetrate the cuticle of intact Eucharis leaves when the tissue below was 
fully turgid but penetration did occur in leaves in which the cells were plas- 
molyzed by sucrose solutions, or killed. Similar results were obtained with 
leaves of Hedera helix, Nerium oleander, and Prunus laurocerasus. Brown 
and Harvey could not explain their results in terms of a chemotropic stimulus 
to penetration, nor in terms of a chemical or enzymic action on the cuticle; 
they could only explain them in mechanical terms and concluded that the 
only stimulus for penetration is contact. 

Robinson (1914) found that germ tubes of a Botrytis sp. were negatively 
phototropic, and Gettkandt (1954) and Jarvis (1972) confirmed this for 
B. cinerea. Gettkandt suggested that this behavior would confer some ad- 
vantage to the parasite in the infection process, but as B. cinerea can infect 
plants in both darkness and light, phototropism would appear to play an 
unimportant part in infection. Borecka, Bielenin, and Rudnicki (1969), how- 
ever, found light to enhance the infection of strawberry flowers from conidia 
of B. cinerea. 

Infection from conidia is fully dependent on the maintenance of a water 
film or drop over the conidium, its germ tube and appressorium (Brown 1915, 
1916; Blackman and Welsford 1916; Brown and Harvey 1927; Jarvis 1962«; 
Borecka, Bielenin, and Rudnicki 1969; and Gartel 1970). Jarvis (1962«) and 
Gartel (1970) showed that, although a water film is essential to germination, 
the further growth of mycelium is less dependent on free water. Others have 
claimed that infection can occur at high relative humidities in the absence 
of free water but these reports are suspect (Schein 1964; and see PART 3, 
"Growth"). However, high relative humidities maintain infection drops in 
the field and so enhance the likelihood of successful infection. Epidemics and 
severe storage rots caused by Botrytis spp. are invariably associated with 
prolonged moist conditions (e.g., Rose 1926; Lauritzen 1930; Baker 1946; 
Nelson 1949, 1951fl, 1951/?; Stalder 1953^; and Tonchev 1972). 

Stevenson (1939) noted that lettuce cotyledons were attacked by B. 
cinerea mainly when the testa remained over them to form a damp incubation 
chamber. 

Shoemaker and Lorbeer (1971) showed that B. squamosa successfully 
attacked onion leaves only if they were continuously wet for at least 6 h and 
that the number of lesions increased significantly for each 3-h interval after 
6 h. Necrosis from the leaf tip downwards increased similarly. Continuously 
wet plants were attacked within the temperature range 9-23 °C. 

67 



Infection can take place very rapidly in many diseases caused by Botrytis 
spp. On strawberry fruits, conidia of B. cinerea began to germinate within 
90 min of inoculation (Hennebert and Gilles 1958) and most had germinated 
in 3-5 h at the optimum temperature of 20°C. However, penetration did not 
occur until about 20 h after inoculation when the second phase of germina- 
tion, germ tube growth, began (see PART 3, "Growth") with its optimum 
temperature of 30°C. The incubation period (sensu van der Plank 1963) was 
thus regulated by two temperature optima. The interval between inoculation 
and the appearance of the first symptom was about 2 days for ripe strawberry 
fruit; this interval included the pre-penetration period for spore germination, 
so the incubation period was about 28 h and the latent period, ended by the 
appearance of conidiophores and conidia, was about 24 h longer. In grapes, 
a latent period of 36 h was recorded by Guillon (1906/?). 

B. elliptica on Lilium candidum produced conidiophores within 7 h and 
conidia within 9 h of rosettes, containing a perennating mycelium, being 
placed in an environment of 18°C and 97% RH (Taylor 1934). The conidia 
were able to germinate within 2 h to initiate secondary infections. 

It might be supposed that flowers, with their secretions from the nectary 
and stigma, would be readily infected, and indeed they frequently are; for 
example Zeller (1926) found flowers of pear to be infected by germ tubes of 
B. cinerea in the stamens, styles, sepals, and sometimes the bracts on pedun- 
cles. He observed infection of epidermal hairs and of stamen filaments. The 
same occurs in strawberry flowers (Jarvis and Borecka 1968); and in grapes, 
B. cinerea infects the stylar end of the flower and becomes quiescent in the 
necrotic stigma and style (Lehoczky 1972; McClellan 1972; McClellan and 
Hewitt 1973; McClellan, Hewitt, La Vine, and Kissler 1973). Nonetheless, 
Jung (1956) examined 1500 inoculated stigmas of 61 species and could find 
no case in which the fungus had penetrated the style as far as the ovary. 
Jarvis and Borecka (unpublished) failed to germinate conidia of B. cinerea 
in undiluted nectar from strawberry and red raspberry flowers, and no report 
of natural infection via the nectary is known. Petals, however, are commonly 
infected (Trojan 1958). 

McWhorter (1939) observed infection by B. cinerea of the glandular 
trichomes on the stem of Antirrhinum ma jus at the junction of the glabrous 
and hirsute zones and suggested that this infection occurred because of the 
water retentiveness of the zone or because of some property of the trichomes. 
Because infection followed insecticide application, infection also might have 
been associated with broken trichomes. 

The infection of tomato petiole stubs reported by Wilson (1963) is 
unique in the literature, but possibly occurs more frequently. In the glass- 
house crop, the lower leaves are usually removed by breaking the petiole or 
cutting it close to the stem, as they wilt and become senescent. In conditions 
of high relative humidity, which often occur at night or in prolonged humid 
weather, drops of water are exuded from the cut surface and the last drop is 
resorbed when transpiration is resumed. If conidia of B. cinerea are present in 

68 



the drop, many of them become lodged in clumps against irregularities in the 
xylem vessels some distance from the surface. There, they may be quiescent 
for as long as 10-12 wk before germinating in situ. The germ tubes then 
penetrate between the bands of spiral thickening into the surrounding paren- 
chyma, which is rapidly colonized (Wilson 1966). 

Many cases of parasitism of Botrytis spp. in woody tissues likely result 
from this type of infection, particularly when symptoms are associated with 
pruning, grafting, or other wounds of, for example, grapevine (Cartel 1964, 
1965fl), black currant (Corke 1969), gooseberry (Rake 1966), and Ribes alpi- 
num (Brierley 191 8fl). In apple shoots, B. cinerea was occasionally associated 
with leaf scars (Swinburne 1973). 

Systemic infection is known only in the clover anther disease (B. antho- 
phila). Conidia, mixed with pollen, invade the flower via the stigma and the 
mycelium reaches the seed to cause systemic infection throughout the life of 
the plant (Silow 1933). Ramazanova (1958ft) also introduced the fungus 
successfully into the growing point. 



Infection from microconidia 

No case is known of infection of plants from microconidia; their only 
role appears to be one of spermatization (see PART 2, "Sexual reproduc- 
tion"). 



Infection from mycelium 

The process of infection from mycelium is essentially the same as that 
from germ tubes (Istvanffi 1905), although, as Jarvis (1962a), Cartel (1970), 
and Bessis (1972) have pointed out, the myceHum almost always has a nu- 
trient-providing saprophytic base. The inoculum potential of mycelium is 
therefore much greater (sensu Carrett 1970) than that of germinating conidia, 
and is also less dependent on the external environment (e.g., the requirement 
for free water in which conidia germinate). Thus Jarvis (1962(3) found that 
only about 1 % of infections of ripe intact strawberry and raspberry fruits 
occurred from conidia germinating in a persistent drop of water on the fruit 
surface; all other infections occurred from mycelia in saprophytic bases of 
some kind. 



Infection from ascospores 

By analogy with the genus Whetzelinia, it seems very likely that asco- 
spores of Botryotinia spp. can infect plant tissues, healthy, senescent and 
moribund, although reports of such infection are few. Codfrey (1923) achieved 
infection of inflorescences of Ricinis communis with ascospores of B. ricini, 

69 



Hainsworth (1949) and Sarmah (1956) found ascospores of B. theae to infect 
the petals of tea flowers, and Vanev (1965) and Kublitskaya and Ryabsteva 
(1970) attributed primary infection of grapevines in the spring to ascospores 
of B. juckeliana, as Bavendamm (1936) did in the case of conifers. 



INFECTIVITY 



Whether or not infection is achieved from conidia depends on many 
environmental factors such as moisture and temperature, but infectivity also 
depends on certain endogenous factors contributing to the inoculum potential 
of the conidia, as qualified by reference to the surface area of the host to be 
infected (Garrett 1970). 

Last, cited by Gregory (1973), estimated that only about 5% of spores 
of Botrytis sp. arriving on leaves of Vicia faba achieved infection; this propor- 
tion is termed 'infection efficiency'. 

Last and Hamley (1956), using a local lesion technique for assessing 
the infectivity of conidia of Botrytis jahae, found that the number of lesions 
on half-leaflets of Vicia faba was directly proportional to the concentration 
of conidia in the infection drop. The variation in lesion numbers between 
plants in a single pot greatly exceeded that between half-leaflets, as did 
variation between leaves of old, but not young, plants. 

In terms of dose-probit responses, that is, the number of spores required 
to produce at least one lesion on 50% of the unit areas of host tissue inocu- 
lated (the ED5Q value), Deverall and Wood {\96\d) found that less than 10 
spores o'f B. fabae were required to give 50% successful inoculations and 
that 10% of single-spore inoculations were successful. Wastie (1962) found 
that the ED5Q value was about 4 spores, and obtained success with 13% of 
his single-spore inoculations. By contrast the ED-o value for spores of B. 
cinerea on Vicia faba was about 500 and only 1 single-spore inoculation in 
116 attempts was successful. Wastie thought that the somewhat larger spore 
of B. fabae could account in part for these differences, which in turn might 
help to explain the natural host-range of the two fungi. 

If the primary lesions, each caused by penetration from a single spore 
of B. fabae, were widely spaced on the leaf, the host defence mechanism 
prevented their further development, but if lesions were sufficiently close 
together, at some critical degree of crowding, there appeared to be some 
synergistic effect between lesions that overcame resistance. 

B. fabae is a vigorous parasite of healthy bean leaves whereas B. cinerea 
is but a weak parasite of healthy leaf tissue and requires special conditions 
to achieve infection, although it readily invades senescent bean tissue such as 
aging flowers and otherwise unhealthy tissue. The infectivity of B. cinerea is 

70 



thus restricted by the particular host tissue attacked and by the physiological 
age and health status of the host. 

Schonbeck (\961a) noted that a low incidence of infection of Fuchsia 
styles in low relative humidities could be increased to some extent by using 
a higher concentration of conidia of B. cinerea. 

Brooks (1908), Brown (1922^), and Deverall and Wood (1961(7), among 
many others, showed that the infectivity of spores of Botrytis cinerea was 
enhanced by the supply of exogenous nutrients. Although Brown found, at 
least in part, that enhanced infectivity was attributable to an increase in the 
proportion of spores germinating. Last (1960^, 1960/?) found that this cause 
could be excluded in explaining the enhanced infectivity of old spores of 
B. fabae on leaves of Vicia jaba. Spores, taken from cultures 25-40 days old, 
germinated equally well in water on bean leaves, but spores 25 days old were 
only one-tenth as infective as young spores and spores 35 days old one- 
hundredth as infective. Their infectivity was partially restored by adding 
orange juice or 0.2% yeast extract to the infection drop, or, more effectively, 
4.5% sucrose (the main carbohydrate component of orange juice), glucose, 
mannose, or maltose. Fructose and galactose were less effective and arabinose, 
xylose, casein hydrolysate, peptone, or nucleic acid did not increase infectivity. 
Abrading the leaves increased the number of lesions when spores were in 
water and the effect was relatively greater with older spores. Honeydew 
secreted by Aphis fabae Scop., which predisposes leaves to infection in the 
field, also increased infectivity, presumably because of its sucrose content. 
Last interpreted these results to mean that aging conidia contain endogenous 
reserves, adequate for germination, but not for overcoming host resistance. 

Using the local lesion technique of assessment. Last and Buxton (1955) 
and Buxton and Last (1956) found that conidia of B. fabae, exposed for 8 h 
to daylight, caused more lesions on half-leaflets of V. faba than conidia kept 
in the dark. The effect was enhanced by keeping plants in the light after inocu- 
lation. When inoculated plants were exposed to ultraviolet light, the propor- 
tion of conidia that infected leaflets increased with the interval between 
inoculation and irradiation. Irradiation immediately after inoculation resulted 
in 3% successful inoculations, an interval of 4 h in 13%, and an interval of 
8 h in 93% successful inoculations. Germination evidently resulted in an 
increase in resistance to irradiation and the fungus was presumed to be pro- 
tected from it after penetration had occurred. Irradiated leaves had increased 
susceptibility, so the same inoculum resulted in more and larger lesions than 
those of the check leaves. 

As a result of ultraviolet irradiation, the infectivity of conidia of B. fabae 
was lost more rapidly than the ability to form colonies on agar. Irradiation 
damage to conidia was mitigated by subsequent exposure to normal daylight, 
both on the host and on agar (Buxton, Last, and Nour 1957). Similarly, Last 
(1960/?) found that fungicide concentrations necessary to inhibit conidial 
germination in a Botrytis sp. were not necessarily those required to inhibit 
infection. 

71 



PREDISPOSITION 



Moribund tissue 

De Bary (1886) and Brooks (1908) early noted that attacks on plants 
by Botrytis cinerea were often associated with prior colonization of dead or 
dying plant debris and that the fungus usually attacked senescent rather than 
healthy tissue. Any factor that provided these conditions, therefore, pre- 
disposed plants to infection — a generality proved many times in specific 
cases. 

Thomas (1921) found that tomato plants sprayed with a suspension of 
conidia of B. cinerea remained healthy for 2 wk in a high relative humidity 
but lesions rapidly appeared if pieces of diseased tissue were used as the 
inoculum. Bewley (1923) and Wilson (1963) also observed enhanced infection 
of tomato stems if the fungus was first established as a saprophyte in badly 
pruned leaf bases, etc. Jarvis (1963) showed that if spores of B. cinerea were 
placed between an adhering petal and the intact surface of a ripe strawberry 
fruit, the petal became fully colonized before infection of the fruit occurred. 
Similarily Kamoen (1972) observed that leaf spot of Begonia caused by B. 
cinerea was invariably associated with a wound or a piece of plant debris. 

Senescent flowers provide an excellent substrate for prior colonization, 
and lesions are often associated with them, either when the flowers are still 
attached to the peduncle or after they have fallen onto some other tissue. 
Such examples are provided by Melchers (1926) for geranium, by Klotz, 
Calavan, and Zentmeyer (1946) for citrus, by Yarwood (1948) for apricot, by 
Hainsworth (1949) for tea, by Beck and Vaughan (1949) for Saintpaulia, by 
Emerson (1951) for red currant, by Leach (1955) for Vicia jaba, by Jarvis 
(1962«) and Jarvis and Borecka (1968) for strawberry and raspberry, by Ford 
and Haglund (1963) for pea, by Kamoen (1972) for Begonia, by Lehoczky 

(1972) for grapevine and berries, by Strider (1973) for statice, by Kikvadze 

(1973) for feijoa, and by Jenkins (1974) for barley. 

Other tissues, becoming senescent naturally or moribund as the result 
of some injury or of malnutrition, are also readily invaded and act as foci for 
the colonization of adjoining healthy tissue. Examples of this type are pro- 
vided by Brown and Montgomery (1948), by Sommer, Fortlage, Mitchell, 
and Maxie (1973), and by Logsdon and Branton (1972) for lettuce; and by 
Johnson (1931) and by Lipton and Harvey (1960) for artichoke attacked by 
B. cinerea; by Valaskova (1963Z?) for tulip leaves attacked by B. tulipae; and 
by Moore and Leach (1968) for bean leaves attacked by B. fabae in the 
aggressive phase. Lipton (1963), however, found that postharvest tipburn in 
lettuce did not result in a higher incidence of decay by B. cinerea. Domsch 
(1957) considered the success of infection to be limited by the nutritional 
reserves of the colonized substrate and by the age of the inoculum; he 
attributed a decline in virulence to the gradual accumulation of inhibitory 
substances as well as to the depletion of food reserves. 

72 



The epiphytic flora has an important influence on infection. Conidia of 
B. cinerea seem to suffer from bacteria in the competition for nutrients (Blake- 
man 1972; Blakeman and Fraser 1971; and Sztejnberg and Blakeman 1973«, 
1973/7). 

There is not always predisposition (q.v.) at the host surface but infection 
is usually assured if moribund host tissue is present. 



Frost 

Temperature is obviously of importance in predisposition and different 
temperatures may affect differentially the growth and infective process of the 
parasite and the growth and defence processes of the host. Thus, Krantz 
(1959) found that pre-inoculation storage at low (3°C) but nonfreezing tem- 
peratures could predispose potato tubers to attack by B. cinerea. Tubers kept 
at 15°C and 24°C before inoculation remained healthy. Stored tulip bulbs 
were found by Doornik and Bergman (1973) to have similar differences in 
susceptibility to B. tulipae at 5°C and 20°C. By contrast, Vasudeva (1930«) 
found that maintaining apples at 30°C for 17 days before inoculation made 
them susceptible to B. allii (B. aclada). He was unable to relate this change 
to changes in content of acid, sugar, or nitrogen. 

Frost damage is a common predisposing factor even if the tissues are 
not badly damaged (Ciccarone 1959). Thus, Abdel-Salem (1934), Brown 
(1935), Brown and Mongomery (1948), Weimer (1943), Halber (1963), and 
Jarvis (1962a) found lettuce, lupins, Douglas fir seedlings, and strawberry and 
raspberry flowers to be so predisposed, particularly if the frost was unseason- 
able. Kerling (1952) grew pea plants in sterile conditions and found that 
B. cinerea or frost alone caused little damage to them, but both together 
caused rapid death. 



Wounds 

Any agent that causes mechanical damage to tissues may facilitate the 
entry of Botrytis spp. Abrasion of bean leaves with diatamaceous earth prior 
to inoculation with conidia of B. fabae enhanced infection, especially by old 
conidia of low infectivity (Buxton, Last, and Nour 1957; Last 1960«); abra- 
sion by wind-blown sand particles may also predispose beans to infection in 
the field. Kerling (1953) noted that sandstorms predisposed peas to foot rot 
caused by B. cinerea and Fusarium avenaceum. 

Sun injury predisposes lettuce to head rot caused by B. cinerea (Abdel- 
Salem 1934). 

Mechanical damage by machinery can also predispose a host to infec- 
tion by B. cinerea, for example, in potato haulm (Harper and Will 1968); 
wind damage similarly can predispose a host to infection by B. cinerea, for 

73 



example, in potato haulm (Grainger 1961) and in raspberry primocanes 
(Jarvis, unpublished). 

The damage caused by snails, slugs, and insects is often followed by 
B. cinerea (Mallet 1973; Voigt 1972). 

Grapes are particularly susceptible to mechanical damage; Francot, 
Geoffroy, and Malbrunot (1956), Branas (1960), Henner (1964), Chaboussou 
(1972), and Lehoczky (1972) list as agents predisposing to B. cinerea: wind- 
blown sand particles, compression between berries, sun, hail, partial severance 
of the grape from its pedicel by pressures within the bunch, other fungal 
lesions, insects, incorrect grafting leading to grape swelling and compaction, 
fungicides, and undue swelling in wet soils. To this list, Vanev (1962, 1965) 
added prior infection by Vncinula necator and the effect of prolonged high 
relative humidities on berry swelling and splitting, and Seguin, Compagnon, 
and Ribereau-Gayon (1969) the depth of rooting, the effect of soil structure 
and the position of the water table on water uptake, and the effect of the 
density of foliage on transpiration. 



Water status 

Tonchev (1972) investigated the role of irrigation in fruit swelling and 
cracking, and the subsequent development of B. cinerea. Over a 9-yr period, 
he established a correlation between berry splitting, the incidence of gray 
mold, and weather conditions during the ripening period. In dry years, irriga- 
tion had no predisposing effect on splitting or gray mold but in wet years 
additional irrigation caused the berries, which then also had a weaker skin, 
to burst and become susceptible to gray mold. Some cultivars were more 
affected than others. 

Nelson (1951«) pointed out that wounds in grapes are probably impor- 
tant in giving the conidia of B. cinerea access to exogenous nutrients and 
water rather than as breaches in a mechanical barrier; in a suitable environ- 
ment the fungus is able to penetrate the intact cuticle anyway, but infection 
is facilitated by the added nutrients (Wilcoxon and McCallan 1934). In wet 
weather, Stalder (1953«) noted the appearance of very fine cracks in the 
cuticle that might be entry points for the fungus. Bessis (1972), by means of 
the scanning electron microscope, also found cracks in the peristomatal areas 
through which infection occurred. 

The water content of tissues is important in predisposing them to infec- 
tion, even if the cuticle is not ruptured. Kerling (1952) considered that the 
entry of B. cinerea into peas is facilitated not only by the increased water: 
air ratio in the intercellular spaces but also by interference with normal 
gaseous exchange; these conditions lead to increased cell permeability com- 
bined with a decreased osmotic pressure. When potato tubers not normally 
parasitized by B. cinerea had their water content increased by 8-9% by 
infiltration, they became susceptible (Mishra 1953). Mishra, as well as Fer- 

74 



nando and Stevenson (1952) and Jarvis (1953), suggested that this suscepti- 
bility could be explained in terms of enhanced diffusion of pectinases; the rate 
of enzyme diffusion was limited by the water content of the intercellular space. 
A similar explanation was made by Vanev (1965) for turgid grape tissue 
parasitized by B. cinerea. 

Reports of increased incidence of gray mold in plants in wet, over- 
irrigated soils (e.g., Wilson 1937; Kirby, Moore, and Wilson 1955; and 
Tonchev 1972) can perhaps be similarly explained, and there may also be an 
effect on the transition of quiescent infections (q.v.). 

Tissue in wet conditions can also be damaged by guttation (Yarwood 
1952; Baker, Matkin, and Davis 1954). Guttation results in the accumulation 
of toxic levels of salts at hydathodes and at the ends of leaf veins, with conse- 
quent tissue necrosis; these areas are then susceptible to infection by B. 
cinerea. In Phaseoliis vulgaris there was a positive correlation between gutta- 
tion and infection (Yarwood 1952). 

In contrast to the general increase in susceptibility as a result of high 
water content, Rubin and Artsikhovskaya (1963) noted that wilting roots of 
sugar beet were less resistant to B. cinerea, and wilting was accompanied by 
an increase in invertase activity. Hering and Manning (1968) found that 
although germination of conidia of B. fabae decreased on wilting leaves of 
Vicia faba, it increased on leaves recovered from wilting as compared with 
check leaves. 



Exosmosis 

In general, conidia germinate better in water on host surfaces than in 
water on inert surfaces in the laboratory, although sometimes they do not 
(Brown 1922«; Wilcoxon and McCallan 1934; Kovacs and Szeoke 1956; 
Chou 1972; Blakeman 1973; Blakeman and Sztejnberg 1973; and Sztejnberg 
and Blakeman 1973^, 1973^). The influence of the host tissues is usually 
mediated by the exosmosis of solutes into the infection drop (Brown 1916, 
\922a). Drops of water lying on various tissues increase in conductivity and 
in those drops containing conidia of B. cinerea, germination is enhanced or 
not, or inhibited, depending on the tissue. The rate of exosmosis is affected 
by the ease of surface wetting and increases rapidly as infection begins. The 
materials entering such drops from grapes have been examined by Kosuge 
and Hewitt (1964); the materials include glucose and fructose in concentra- 
tions as high as 5 X 10 ^ M, which are stimulatory to conidia of B. cinerea, 
together with amino acids, which have no marked effect. Sol (1969) demon- 
strated the transfer of ^^C from leaf photosynthate to conidia of B. fabae 
via leaf exudates. Sol (1966, 1967, 1968, 1969) pretreated leaves of Vicia 
faba in various ways to increase exosmosis and hence infection by B. fabae. 
The treatments included contact with sucrose, potassium chloride, lathanum 
chloride, ammonium sulfate, and calcium chloride solutions or simply keep- 
ing leaves in the dark. Cell permeability was also increased by alkenyl suc- 

75 



cinic acids, and especially by decenylsuccinic acid, which induced the ex- 
osmosis of sugars and amino acids and resulted in a higher rate of spore 
germination and more lesions. 

Kovacs and Szeoke (1956) considered that persistent rain and dew films 
on leaves often contained enough solutes to exert an effect on conidial 
germination. Aphid honeydew may likewise predispose leaves to infection 
because of its sugar content (Last 1960<3; Sode 1967). 

Fungi not normally parasitic on a given host may be induced to become 
so by adding nutrients to the infection drop; thus B. allii (B. aclada) and B. 
cinerea were induced to attack apple fruits by adding nitrogen salts; the 
addition apparently also stimulated the production of pectinases (Vasudeva 
1930a; Chona 1932). 

Yarwood (1959) noted that adding sucrose to the substrate of detached 
leaves of Vicia faba reduced the size but not the number of lesions caused 
by B. fabae. 

If water into which the nematode AnguilluUna dipsaci had secreted en- 
zymes was used in the inoculation of onion by B. allii (B. aclada), infection 
was enhanced, as it was in the similarly predisposed infection of cabbage by 
B. cinerea (Myuge 1959). 



Volatile metabolites 

In addition to the effects on conidia of direct exomosis from various 
tissues, Brown (1922ft) noted that germination can also be affected by volatile 
materials coming from tissues. Volatiles from potato tubers and onions were 
inhibitory to conidia of B. cinerea, as were those from moist filter paper 
often used in incubation chambers. Other tissues emitted substances that 
stimulated germination, and their effects could be simulated by certain esters. 
Schiitt (1973) found that volatile materials from the leaves and shoots of 
various Coniferales either stimulated or retarded the germination of conidia 
of B. cinerea and, to a lesser extent, mycelial growth. The effect of volatiles 
from Abies alba, Picea abies, Pinus sylvestris and Pseudotsuga menziesii was 
more marked in the light than the dark, and more so at 20°C than 6°C. 
Volatiles from Pseudostuga taxifolia at — 6°C stimulated germination, whereas 
at 20°C they inhibited it. 

Smith, Meigh, and Parker (1964) and Nichols (1966) found that ethylene 
in concentrations of the order of 0.06 ppm could predispose flowers to infec- 
tion by B. cinerea and induce further ethylene production from carnations. 
The removal of ethylene from the storage atmosphere by potassium perman- 
ganate, for example, not only retards ripening of Chinese gooseberries (Acti- 
nidia chinesis) but reduces the incidence of postharvest rots (Strachan 1968). 

Ozone injury was similarly found by Manning, Feder, Perkins, and 
Glickman (1969) and Manning, Feder, and Perkins (1970) to predispose 

76 



_ 



potato and geranium leaves to infection by B. cinerea; and Chrysanthemum 
flowers were predisposed by smoke and insect damage (Taylor and Muskett 
1959). In parentheses and conversely, prior infection by B. cinerea protected 
Vicia faba against visible ozone damage (Magdycz and Manning 1973). 

McWhorter (1939) noted that attacks by B. cinerea on Antirrhinum 
majus occurred after applications of insecticides for thrips control; the insec- 
ticide seemed to predispose trichomes to infection, possibly because of chem- 
ical or mechanical injury or because of water retention in that zone. 

An interesting interaction between B. cinerea, Vncinula necator (powdery 
mildew), and fungicides on grapes was noted by Kundert (1963). Plots were 
sprayed or not sprayed with a sulfur-dinocap mixture to control powdery 
mildew; superimposed on these treatments were sprays of copper oxychloride, 
or of a copper-dinocap mixture, or of dinocap alone. In all plots receiving 
dinocap, the incidence of gray mold increased during the season, although 
powdery mildew was as well controlled as by the copper oxychloride alone. 
Grapes sprayed with copper oxychloride had thick, russetted skins and al- 
though they tended to split open, leaving an apparently ideal site for infec- 
tion by B. cinerea, they ripened very slowly and were less often infected than 
grapes receiving dinocap. Dinocap controlled powdery mildew but it induced 
very thin skins, which split open easily, and it prolonged the ripening period 
during which the grapes remained very susceptible to B. cinerea. Grapes with 
uncontrolled powdery mildew remained small and fairly thick-skinned, and 
they failed to ripen; they remained resistant to B. cinerea. 



Carbohydrate status 

The effect of sugar content of tissues on their susceptibility to attack by 
Botrytis spp. has been examined by many workers. Horsfall and Dimond 
(1957) classified Botrytis spp. as 'high-sugar' pathogens, that is, they usually 
attack tissues with a high sugar content, especially of reducing sugars. Thus 
grapes, both cultivars and individual berries within the bunch, are predisposed 
to B. cinerea (Roemer, Fuchs, and Isenbeek 1938; Nelson 1949, \95\a\ 
Branas 1960; and Chaboussou 1972). Although Cosmo, Liuni, Calo, and 
Giulivo (1966) could not confirm this, they did obtain a positive correlation 
between susceptibility and total acids and a negative correlation with pH; 
but these correlations also are contrary to the experience of Home (1932, 
1933) and Home and Gregory (1928) with B. cinerea on apples. 

Kristoflferson (1921) found a correlation between the incidence of stor- 
age rot in carrots and the reducing sugar content of four cultivars. 

Kamoen (1972) found that Begonia leaves with a high sugar content 
were particularly susceptible to infection by B. cinerea via damaged tissues 
and that infection could be reduced, in part, by shading to depress the rate 
of photosynthesis. Barash, Klisiewicz, and Kosuge (1963, 1964) found that 
reducing sugars leached from flowers of safflower stimulated both the germina- 

77 



tion of conidia of B. cinerea and the production of polygalacturonase, xyla- 
nase, cellulase, and pectin methylesterase, and similarly Orellana and Thomas 
(1962) related susceptibility to B. ricini of castor-bean capsules to levels of 
leachable sugars. 

In contrast, Sukhorukov, Gerber, Barabanova, and Borodulina (1933) 
and Sukhorukov (1957) found that cabbage leaves deprived of sugars were 
more susceptible to B. cinerea, although the method used (keeping the plants 
in darkness) may have induced fairly drastic changes in metabolism and 
perhaps senescence. 

A general theory about the role of carbohydrates in predisposition has 
been elaborated by Grainger (1956, 1962^, 19626, 1968). He thought that 
the carbohydrates surplus to the host's metabolic requirements stimulated 
infection, because they were available to the pathogen and aided its devel- 
opment. He evolved the C„:Rs ratio as a measure of this, where C,, is the 
total carbohydrate content of the plant and Rs the residual dry weight of the 
shoot. This concept seems applicable to a wide variety of host-parasite com- 
binations; when the ratio exceeds 0.5, plants are regarded as susceptible and 
above 1.0 an epiphytotic may be expected. Very young seedlings have a high 
CpiRs value giving them hypersensitivity; slightly older plants have a low 
value and high resistance; and maturing plants have an increasing CpiR^ ratio 
and increasing susceptibility. Grainger has obtained good agreement for his 
hypothesis from individual strawberry fruits, which are formed in succession 
on a cymose inflorescence and are decreasingly susceptible to B. cinerea, 
as well as from tomato — B. cinerea, Vicia faba — B. cinerea and B. fabae, 
narcissus — B. narcissicola, tulip — B. tulipae, gooseberry fruits — B. cinerea, 
and onion — B. allii (B. aclada). 

Possibly changing metabolism in maturing tissues likewise affects the 
transition of quiescent and latent infections to an aggressive state (see PART 
4, "Quiescent Infections"). 

Many fungicides, pesticides, herbicides, and growth regulators alter the 
metabolism of the host, thus changing its susceptibility; many such cases have 
been explained in terms of altered sugar status. Zinc and carbamate fungicides 
were noted to increase the incidence of B. cinerea as a tomato pathogen 
(Darby 1955; Cox and Hayslip 1956; Harrison 1961; and Lockhart and 
Forsyth 1964) and as a grape pathogen (Stellwaag-Kittler 1964; Chaboussou 
1970). Lockhart and Forsyth suggested that maneb and zineb stimulate the 
release of nutrients to the fungus. Zineb also predisposes onion to attack by 
B. allii (B. aclada) because, van Doom (1959) suggests, of the prolonged 
ripening period. Crowdy and Wain (1950) found that 2,4,6-trichloro- and 
pentachlorophenoxyacetic acids, pentachlorophenoxy-/5o-butyric acid, and a- 
(2-naphthyl)-phenylacetic acid checked the spread of individual lesions of 
B. cinerea on Vicia faba but not the number of lesions, an effect ascribed by 
van der Kerk (1963) to alterations in carbohydrate metabolism of the host. 
Corke (1969) considered that some fungicides may stimulate detoxification 
mechanisms. 

78 



Many herbicides interfere with carbohydrate status: lettuce became 
highly resistant to B. cinerea following the application of 2,4-dichloro- 
phenoxyacetic acid and MCPA (Wagner 1955) and Vicia faba became highly 
resistant to B. fabae after 2,4-D (Mostafa and Gayed 1956; Gayed and 
Mostafa 1962); Grummer (1963) obtained a close correlation between the 
incidence of B. fabae on beans and the dose rate of simazine, which inhibits 
the Hill reaction, and Orth (1967) found that chlorpropham increased the 
susceptibility of tulips to B. tulipae. Davis and Dimond (1953, 1956) dis- 
cussed the similar role of growth regulators in altering disease resistance, and 
Smith and Corke (1966) obtained good control of B. cinerea on black currant 
with (2-chloroethyl) trimethylammonium chloride, as did Natalina and Svetov 
(1972a) on grapes. Moore and Leach (1968) used 6-benzylaminopurine to 
delay senescence of bean leaves and hence the onset of the aggressive de- 
velopment of B. fabae. However, senescent leaves were attacked more ag- 
gressively after this treatment, as were senescent leaves in wider plant- 
spacings. 



Nitrogen 

Chaboussou (1970) noted an increase in the incidence of B. cinerea on 
grapes treated with DDT and attributed the increase to an increased nitrogen 
content of the berries (see also "Fertilizers" below). 



Light 

Light affects the carbohydrate status of plants and also other metabolic 
processes of both host and pathogen. Excessive shade predisposes glasshouse 
tomatoes to B. cinerea (Bewley 1923), as does snow and mulch cover in the 
case of Douglas fir seedlings attacked by Botrytis sp. (Sato, Shoji, and Ota 
1959). On the other hand, Segall and Newhall (1960) found that B. allii 
caused lesions on onion leaves only in the light and Borecka, Bielenin, and 
Rudnicki (1969) obtained more infection of strawberry flowers by B. cinerea 
in the light than in the dark. Kamoen (1972) noted the same for Begonia 
leaves and attributed a higher incidence of infection by B. cinerea to a 
higher sugar content of the leaves in bright light; the higher sugar content 
also led to a greater production of the toxin citric acid. Exposure to ultra- 
violet light had no effect on the incidence of B. cinerea in lettuce (Sirry 
19576) but resulted in more infection of Vicia faba by B. fabae (Buxton and 
Last 1956). Bazzigher (1953) found antibiotic activity against B. cinerea in 
Phaseolus vulgaris to be enhanced by light and decreased by darkness. 

Ultraviolet irradiation of bean leaves before inoculation with conidia 
of B. fabae increased the proportion achieving infection (Buxton, Last, and 
Nour 1957). 

79 



Microorganisms 

Predisposition may be eflfected by prior damage to plants by other fungi; 
for example, B. cinerea was frequent on lesions of Puccinia asparagi on 
asparagus (Ogilvie, Croxall, and Hickman 1939) and on lesions of Puccinia 
antirrhini on Antirrhinum sp. (Baker 1946), on lettuce attacked by Bremia 
lactucae (Smieton and Brown 1940; Louvet and Dumas 1958) and by 
Pythium sp. (Basile 1952), on sunflower heads attacked by Whetzelinia 
(Sclerotinia) sclerotiorum (Crisan 1964), on Pelargonium zonale attacked by 
Cory neb acterium fascians (Maas Geesteranus, Koek, and Wegman 1966), on 
grapevine attacked by Uncinula necator (Boubals, Vergnes, and Bobo 1955; 
Branas 1968; and Vanev 1962), on grapevine following the application of 
non-copper fungicides for the control of Plasmopara viticola (Emiliani 1963; 
Stellwaag-Kittler 1964), and on Saintpaulia injured by mites (McDonough 
and McGray 1957). Similarly, B. squamosa was often associated with Pero- 
nospora destructor on onion (Hickman and Ashworth 1943), and B. glohosa 
with aecidia of Melamspora sp. on Allium ursinum (Hennebert 1958). 

Prior infection by the pea leaf roll virus has been observed to predispose 
bean plants to B. cinerea (Tinsley 1959). 

Powell, Melendez and Batten (1971) found that tobacco plants, exposed 
to the nematode Meloidogyne incognita for 4 wk, were unusually susceptible 
to B. cinerea. 



Pollen 

The presence of pollen grains in the infection drop affects spore germina- 
tion (Brown 1922fl) and is often associated with increased infection by B. 
cinerea; such an increase has been noted on stone fruit blossoms (Ogawa and 
English 1960), on holly flowers (Batchelder and Orton 1962), on strawberry 
flowers and fruit (Jarvis and Borecka 1968; Chou and Preece 1968; and 
Borecka, Bielenin, and Rudnicki 1969), on Begonia leaves (Kamoen 1972), 
on grape flowers (McClellan 1972; McClellan and Hewitt 1973), and on 
spikelets and leaves of barley (Jenkins 1974). This effect is attributed, at least 
in part, to the relatively high content of abscissic acid in pollen and other 
floral parts (Borecka and Pieniazek 1968; Borecka et al. 1969) and possibly 
to the presence of bacteria in the pollen (Borecka, unpublished). In some way, 
pollen also enables the fungus to overcome the antibiotic effects of wyerone 
acid in Vicia faba (Mansfield and Deverall 1971). Strange, Majer, and Smith 
(1974) thought that choline and betaine, two major components of wheat 
anthers that stimulate Fusarium avenaceum, were not involved in the pollen 
effect on B. cinerea, but they did find that a wheat-germ extract could increase 
the virulence of B. cinerea on bean leaves. 

80 



Fertilizers 

The nutritional status of plants greatly affects the incidence of Botrytis 
spp. (Krauss 1969), especially deficiencies leading to premature senescence. 
Examples of deficiencies that increase the incidence of disease are: 

N, P, K, Mg B. cinerea (Brooks 1908) 

P, K B. fabae on Vicia faba (Glasscock, Ware and Pizer 1944; 

Moore 1944; Furse 1949; Leach 1955) 

K B. cinerea on potato (Harper and Will 1968) 

K B. cinerea on grape (Pevov, Chepelenko, Perova and 

Ilyashenko 1973) 

K B. cinerea on peas (Wijngaarden and Ellen 1968) 

K, Mg B. tulipae on tulip (Valaskova 1963Z?) 

Conversely, excessive nitrogen in particular may predispose in some cases: 

B. cinerea on strawberry (Darrow and Waldo 1932; Vukovits 1962) 
B. cinerea on stored nursery stock (Haas and Wennemuth 1962) 
B. cinerea on Chrysanthemum morifolium (Hobbs and Waters 1964) 
B. cinerea on grapevine (Delas 1972) 
B. alia on onion (Vaughan 1960) 

One effect of excessive nitrogen is usually an excessive vegetative growth 
that produces microclimates conducive to infection, and, as Delas (1972) 
pointed out, similar effects could be obtained by other cultural modifications. 
Delas considered that the predisposing effects of excessive nitrogen result less 
from higher nitrogen content in grape berries than from other changes in the 
physiology of the whole plant. By contrast, Meriaux, Libois, N'Guyen van 
Long, Biol, Naudin, and Collin (1972) could find no effect of higher nitrogen 
applications in a young vineyard on the incidence of gray mold over a 3-yr 
period, and only a slight increase in the nitrogen content of the berries. 

Verhoeff (1968) found that increasing the level of soil nitrogen decreased 
the incidence of stem gray mold in tomatoes; in this case the increased nitro- 
gen probably delayed senescence and hence the development of latent in- 
fections (q.v.). 

Calcium in correct amounts usually confers some resistance (q.v.) on 
plants, probably partly because of its effect on the structure of cell walls. 
Calcium deficiency is reported to increase gray mold of beans (Deverall and 
Wood 1961) but Knoblauch (1958) reported an increase in the incidence of 
B. alia on shallots treated with calcium nitrate. 

The incidence of the chalky-seed condition in pea seed was correlated 
with the incidence of attack by B. cinerea (Sode 1971). 

81 



In soils having a pH below 5.0, Sirry (1953, 1956, 1958) found B. 
cinerea to be more severe on lettuce and potato, B. fabae more severe on 
beans, and B. allii more severe on onions. Grainger (1968) found that the 
strawberry cultivar Templar was least severely affected by B. cinerea when 
the soil pH was 5-5.5, and the cultivar Cambridge Vigour at soil pH of 5.5-6. 

The enrichment of air in a tomato glasshouse with carbon dioxide has 
been reported (Anon. 1967) to result in a higher incidence of B. cinerea, but 
this effect could have resulted from an unsuitable microclimate in the poorly 
ventilated house; the foliage was also considerably denser than in an un- 
enriched house and may have had a higher sugar content. 

Trace elements have some effect on the general health status of plants 
as well as perhaps on resistance mechanisms and the fungus; Timchenko 
(1957) found boron and copper to decrease the incidence of B. cinerea on 
sunflower and Brandenburg (1942) noted that B. cinerea was secondary on 
boron-deficiency lesions on cauliflower and kohlrabi. 



PATHOGENESIS 



Most species of Botrytis, with the possible exception of B. convoluta 
(Maas and Powelson 1972), secrete pectic enzymes and other enzymes that 
degrade cell walls; the host cells die, and hyphae pass through infected tissue, 
starting along the lines of middle lamellae (Ward 1888; Wood 1960; and 
Brown 1948, 1965). The net result is that having achieved entry into the 
host, the fungi live saprophytically on the dying and dead host tissues, almost 
always parenchyma, and continue to colonize tissues at the edge of the lesion. 
However, hyphae never parasitize healthy tissues in the sense that obligate 
fungi do; hyphal tips are some distance behind their excreted enzymes and 
toxins and so always in moribund tissue. The fungi thus continue to build 
up a saprophytically based inoculum potential both for continued coloniza- 
tion by hyphae and for sporulation. In the case of B. cinerea, and probably 
other species, the process of degradation evidently continues on the dead 
shoot (Hudson 1968) and in the soil with the aid of cellulases, pectinases, 
cutinase, and other enzymes (see PART 1, "Introduction"). 

Histologically, the distribution of mycelium in strawberry fruits invaded 
by B. cinerea has been described by Stevens (1916) and Powelson (1960), in 
grape berries by Istvanffi (1905) and Nelson (1956), and in dry and fleshy 
onion scales by Clark and Lorbeer (1973<3, 1973ft). In all of these, the hyphae 
penetrate mostly along the line of middle lamella but eventually the cell 
walls, in various stages of degradation, are penetrated, sometimes apparently 
mechanically. Often cells are entered at the junction of two neighboring 
cells. In grapes, early separation of the epidermis from the underlying tissues 
gives the condition 'slipskin' (Barretto 1896) and Nelson found that the 

82 



periclinal cell walls were disrupted more readily than anticlinal walls, prob- 
ably because of component differences in their respective pectins. Brown 
(1915) had also attributed differences in the action of the macerating factor 
to structural differences in the cell walls. 



Enzymes 

A major difficulty in work on the pectinase complex has been to 
correlate in vitro activity of the various enzymes with their role in infection 
and pathogenesis. Probably only the ill-defined protopectinase or 'macerating 
factor' (Byrde and Fielding 1962) is of immediate pathogenic importance in 
host-cell separation and the remaining factors are of greater significance in 
the nutrition of the fungi during their saprophytic phase (Peltier 1912); see 
PARTI, "Introduction". 

Brown (1915), Tribe (1955), and Fushtey (1957) were never able to 
separate the macerating and toxic activities in preparations from B. cinerea. 
By growing B. cinerea for varying periods in media containing different pro- 
portions of pectin and glucose, Jarvis (1953) obtained culture filtrates with 
differential pectinase activity and hence circumstantial evidence that the 
macerating activity is distinct from polygalacturonase, pectin methylesterase, 
and depolymerase. Further, macerating activity on potato-tuber discs was 
maximal at pH 2.6 and at pH 6.2, which agreed with the pH optima for the 
pectin viscosity-reducing enzyme depolymerase, but not with the pH optima 
for pectate depolymerase. Evidence from thermal inactivation also indicated 
the distinction between macerating activity and other pectinase activity. The 
relationship between maceration and pectinase activity was also examined 
by Kaji, Tagawa, and Yamashita (1966). They found pH optima of 3.0 and 
5.0 for a culture filtrate from B. cinerea macerating potato tissue, and pH 
optima of 1.5 and 4.5 for the bark tissue of Wikstroemia sikokiana. A 
bimodal response was also found for endopolygalacturonase, at pH 3.6 and 
5.4, but only one peak for exopolygalacturonase at pH 5.0 and one peak for 
pectin methylesterase at pH 3.5-4.5. They concluded that macerating 
activity was probably the result of joint action of endopolygalacturonase and 
pectin methylesterase. 

Tani and Nanba (1969) identified 3 kinds of macerating activity among 
culture filtrates from 10 isolates of B. cinerea: one enzyme had a pH optimum 
at 2.7, like Jarvis' enzyme; a second had its optimum at pH 5.5 and was 
inactivated at low pH values; and the third degraded mitsumata inner bark 
but not potato tissue and was also inactivated at low pH. 

Maceration of parenchyma can occur very rapidly and is probably ac- 
complished primarily by breaking lateral linkages of divalent ions or hydrogen 
bridges between parallel pectic and other carbohydrate chains and possibly 
protein chains (Ginzburg 1961; Joslyn 1962), rather than by the action of 
enzymes decreasing chain length. However, no proteinase activity was de- 
tected by Porter (1966) in apple and tomato fruits infected by 2 isolates of 

83 



B. cinerea, although proteinase activity was detected in cultures of B. cinerea 
by Lyr and Novak (1962), Tseng and Lee (1969), and Astapovich, Babitskaya, 
Hrel, and Vidzischchuk (1972). 

In Monilinia fructigena, also a soft-rotting fungus, maceration has been 
attributed to pectin methyl-/ra/i^-eliminase (Byrde and Fielding 1968) but 
the enzyme is thought to act on the substrate in the host-cell membrane or 
in the protoplast (Mount, Bateman, and Basham 1970). 

Verhoeff and Warren (1972) found that enzyme activity varied in tomato 
plants parasitized by B. cinerea', pectin methylesterase, endo- and exopoly- 
galacturonase activity was detected in petioles and fruit, but cellulase was 
detected only in those parts softened by the advancing fungus. Polygalactu- 
ronate trans-e\imimLse was found only in the softened areas of petiole stumps. 
Verhoeff and Warren considered that B. cinerea itself produced all the 
enzymes necessary for pathogenesis in tomato. 



Toxins 

The cytoplasm of cells is killed before fungal hyphae advance into dead 
tissues (de Bary 1886; Ward 1888; Nordhausen 1899; Brown 1915; Stevens 
1916; Menon 1934; Bocharova 1940; Jefferson, Davis, Baker, and Morishita 
1954; Akai, Fukutomi, Ishida, and Kunoh 1966; Tichelaar 1969; Cartel 
1970; and Jamart and Kamoen 1972), which are then digested by the fungus 
(Peltier 1912; Talieva and Plotnikova 1962). Smith (1902) proposed that the 
toxin responsible was oxalic acid, but Peltier (1912) and Brown (1934, 1936, 
1965), reviewing the evidence, felt that the toxin was not oxalic acid, but was 
either the macerating factor or so closely linked to it as to defy separation 
(Tribe 1955; Fushtey 1957; Byrde and Fielding 1962; and Tseng and Mount 
1974). B. cinerea, however, is capable of producing oxalic acid in culture 
(Gentile 1954; Jamart and Kamoen 1972; and Kamoen 1972), as is B. allii 
and possibly B. globosa (Hellmers 1943). 

Kamoen (1972) and Jamart and Kamoen (1972, 1974^) found citric 
acid in culture filtrates of B. cinerea, sometimes with oxalic acid, and in sap 
expressed from Begonia leaves and containing conidia. Citric acid also oc- 
curred in yellow tissue of infected leaves, that is, in the zone containing 
hyphal tips and extending a little beyond them. Citric acid reproduced the 
yellowing symptom in leaves (Kamoen 1972; Kamoen and Jamart \91Aa) 
and so satisfied the criteria for a vivotoxin as defined by Dimond and Wag- 
goner (1953). 

Kamoen (1972) proposed a hypothesis for pathogenesis by toxins in 
Begonia leaves. The cell walls contain a certain amount of water, depending 
on the plant's environment, and corresponding films of water of various 
thicknesses on the walls bounding intercellular spaces. The thickness of the 
film, which tends to be greater in the yellow zone because of increased cell 
permeability, largely determines the rate of enzyme and toxin movement in 

84 



advance of the hyphae (as Jarvis 1953 had also suggested for pectinases). As 
conditions become drier, the translucent, water-soaked appearance of the 
yellow zone disappears and fungal activity slows. Eventually, a dark zone 
appears at the edge of the green tissue and fungal development is stopped. 
In resumed wet conditions, this barrier can be breached in a few points, from 
which fungal invasion begins again. 

Toxins, other than citric and oxalic acids, have frequently been invoked 
in many disease situations, particularly by many Russian workers in the 
pathogenesis of B. cinerea on cabbage (Rubin and Artsikhovskaya 1963). 
Artsikhovskaya and Rubin (1937) noted that a zone of cell death extended 
beyond the hyphal zone, especially in the susceptible cultivar No. 1. Ovcarov 
(1937) considered that thiourea accumulating in tissues parasitized by B. 
cinerea could account for yellowing of leaves and a reduction in photo- 
synthetic activity. Gentile (1951), Sautoff (1952, 1955), and Bazzigher (1953), 
obtained toxins in culture filtrates of B. cinerea. Krasil'nikov (1952) found 
that honeydew became phytotoxic after B. cinerea had grown in it. Bran 
cultures of B. cinerea induced some browning and soft rot in tomato stems, 
in common with many other wilt and root-rot pathogens, which Winstead and 
Walker (1954) thought to result from pectin methylesterase activity. 

Purkayastha (1969, 1970) obtained culture filtrates from both B. cinerea 
and B. fabae that caused wilt and necrosis of cut shoots of Vicia faba, as well 
as browning of the primary root and softening of the root tip and of stem 
segments. Wilting was accompanied by vascular plugging and browning of 
the vessel walls. The active principles were non-dialysable and partially ther- 
molabile, and their activity was influenced by culture conditions. Purkayastha 
(1969, 1970) also detected phytotoxicity in Botrytis-'miQciQd bean leaves. 

Kamoen and Jamart (1974^) found a phytotoxic polysaccharide in 
Begonia leaves attacked by B. cinerea. 

The biochemical effects of toxins produced by B. cinerea in cabbage 
tissues have been examined extensively by Rubin and his students (Rubin and 
Artsikhovskaya 1963). In general the toxins, resolvable into polysaccharide 
and acid fractions, interfere with oxidative processes (Chetverikhova 1952; 
Krasil'nikov 1953; Ladygina and Rubin 1957; Ladygina 1962; Aksenova 
1962, 1964; Artsikhovskaya 1946; Rubin and Aksenova 1964; and Rubin and 
Ladygina 1964); thus the toxins increase invertase, peroxidase, and cyto- 
chrome oxidase activities and oxidative phosphorylation in affected tissues 
and induce the synthesis of enzymes and other proteins (Rubin, Aksenova, 
and Brynza 1973; Rubin, Aksenova, and Kozhanova 1973; and Rubin, 
Aksenova, and Nguyen Din Guen 1971^, 1971^). The identity of compo- 
nents is still unknown, as is their relation to Brown's toxin. 

The effects of Botrytis species on plant anatomy and metabolism are 
complex and probably vary with each host-parasite combination (Akai, 
Fukutomi, Ishida, and Kunoh 1966). B. allii (B. aclada) secretes substances 
in advance of the hyphae; these substances reduce nuclear size in epidermal 
cells of onion bulb scale leaves, and the effect decreases with distance from 

85 



the inoculum, up to 2 cm. Nuclei in contact with hyphae disintegrate. Culture 
filtrates also cause nuclear disintegration and reduction in DNA content 
(Kulfinski and Pappelis \91\a, \91\b; Kulfinski, Pappelis, and Pappelis 
1973; and Somasekhara and Pappelis 1973). The toxin of B. cinerea also 
causes a reduction in nuclear size in cabbage (Aksenova 1964), especially in 
the susceptible cultivar No. 1 . 

Ilieva (1971) considered that toxins from B. cinerea were responsible 
for initiating abscission of inoculated tomato petioles. 

Evidence of considerable metabolic activity in apple fruits infected by 
B. cinerea was adduced by Fischer (1950); the temperature at a distance of 
0.6 cm from the point of infection was 0.06°C higher than at a distance of 
2.1 cm and 0.09°C higher than at a greater distance. 

Lesions caused by Botrytis spp. and especially by B. cinerea often have 
a water-soaked appearance and Yarwood (1966) showed that water did 
indeed accumulate in broad-bean tissues infected by B. cinerea. 



Restricted lesions 

Understanding the pathogenesis of Botrytis spp. on onion has long pre- 
sented problems. Yarwood (1938) found that oval, whitish-gray lesions on 
living leaves and flower stalks of onion were sterile, although on dead 
material B. cinerea usually spored. The symptoms were reproduced by inocu- 
lation and when conditions for infection were good, lesions merged eventually 
to cause wilt and death from the leaf tip down. Yarwood considered this to 
be analogous to chocolate spot of beans and ghost spot of tomato, and another 
example of nonaggressive infection. Segall (1953) found that while onion 
blast or leaf spotting could be caused by various Botrytis spp. including B. 
alia (B. aclada), B. cinerea, B. tulipae, and B. paeoniae by inoculation, only 
B. alia could be found in the field in New York State, sporing on dead foliage, 
but not on leaf spots. Further, Segall could find no evidence that penetration 
had occurred through the cuticle or stomata, and Segall and Newhall (1960) 
could not isolate the fungus from leaf spots, nor find mycelium in the tissues. 
Leaf spots were formed when spores were placed on the leaf but only in the 
presence of light, and the spot apparently resulted from the separation of the 
epidermal cells from the palisade layer. Eventually the parenchyma became 
disorganized. Spots were also induced by a toxin in culture filtrates, in both 
darkness and light, and germinating spores were thought also able to secrete 
a toxin. This finding is in contrast to the conclusion of Brown (1915) that 
spore secretions by B. cinerea do not act if the cuticle remains intact. Perhaps 
the onion cuticle differs in some way from those studied by Brown (mainly 
petal cuticles); Scott, Hamner, Baker, and Bowler (1957, 1958) thought 
plasmodesmata were continuous right through the wall and cuticle of onion 
epidermal cells. If so, toxins could reach the cytoplasm through them; further 
work in this area is obviously necessary. 

86 



Hancock, Millar, and Lorbeer (1964) tried to explain the earlier obser- 
vations of Hancock and Lorbeer (1963) on the pathogenesis of B. cinerea, 
B. squamosa, and B. allii on onion. In New York State, B. squamosa and 
B. cinerea were the most prevalent: the former caused elliptical lesions 
throughout the leaf and eventually dieback from the tips; the latter caused 
more superficial leaf flecks. All three fungi produced pectin methylesterase and 
cellulase in potato dextrose broth, detached onion leaf sections, and leaves 
of intact plants. B. allii produced a trace of polygalacturonase in broth, but 
more in leaves; B. cinerea produced a very active polygalacturonase in broth 
and leaves, and B. squamosa produced exopolygalacturonase only in de- 
tached leaves and endopolygalacturonase in broth and leaves. 

A somewhat similar situation was thought to prevail in tomato ghost spot 
(a small necrotic spot surrounded by a light-colored halo). For many years, 
attempts to isolate a fungus from the spots were unsuccessful (Bewley 1923; 
Ainsworth, Oyler, and Read 1938; Darby 1955; Owen and Ferrer 1957; and 
Ferrer and Owen 1959). Ainsworth, Oyler, and Read reproduced the disease 
by inoculation; Owen and Ferrer were the first to demonstrate the presence 
of B. cinerea in the spots, but only Verhoeff (1970) succeeded in isolating it. 
Ainsworth et al. thought that the symptoms were produced by the germ tubes 
penetrating the cuticle of immature fruits, secreting pectinases and thus 
separating the epidermis from the underlying tissues; the air gap so formed 
produced the halo effect. Verhoeff reexamined ghost spot and found that pe- 
netration did indeed occur. No mycelium could be found in the necrotic cells, 
though their dense contents make observations difficult; however, the fungus 
could be isolated from them. He obtained typical symptoms by inoculating 
fruits with only a few dry conidia. With many conidia, however, scab-like 
lesions resulted and, under conditions of high relative humidity, large blisters 
were formed before the fungus spread through the parenchyma. Under con- 
ditions of low humidity, necrotic areas appeared. Verhoeff thought it possible 
that meristematic activity of the rapidly expanding fruit limited the growth 
and enzymatic activity of the fungus in normal growing conditions but failed 
to limit them when conditions were very humid or when many conidia were 
used as the inoculum. He considered ghost spot as an example of latency 
(q.v.). 

The blistering noted by Verhoeff in tomato fruits is paralleled by that 
noted by Beaumont, Dillon Weston, and Wallace (1936) on tulip flowers 
infected by B. tulipae in very humid conditions. 

Nelson (1949) observed a banded appearance on infected grape berries 
and distinguished 3 zones: the outer, light-colored zone represented separa- 
tion of the epidermis from the underlying tissues (reminiscent of tomato 
ghost spot and onion blast); the middle zone, dark and circular, was an area 
of dead protoplasts; and the inner translucent zone was one of further dis- 
organization. Cartel (1970) also observed repetitive parallel banding of this 
type on grape berries but he considered that differences in temperature be- 
tween day and night were responsible. During the night, the fungus grows 
slowly, forming stout, closely packed hyphae that show through the cuticle 

87 



as a dark zone; during the warmer days, thin, unbranched hyphae are formed 
that are hardly visible through the cuticle. This banding is also characteristic 
of lesions caused by B. cinerea on raspberry canes (Jarvis 1962a) and of 
those caused by B. cinerea on Begonia leaves (Jamart and Kamoen 1972), 
although whether these bands are caused by different types of cell degrada- 
tion or by different types of fungal growth is unknown. 

Kamoen (1972) suggested that the zones on Begonia leaves resulted 
from periods of fast hyphal growth and enzyme production in wetter condi- 
tions, alternating with periods of slow hyphal growth and toxin production in 
drier conditions. 



Osmotic relations 

B. cinerea can tolerate great osmotic pressures (Hawkins 1916; Weimer 
and Harter 1921; and Rippel 1933^) and Thatcher (1939, 1942) formed a 
hypothesis in terms of osmotic relationships between the fungus and its host 
(in this case celery petiole tissue) to explain the pathogenicity and nutrition 
of the fungus. He found that the osmotic pressure of hyphal cells of B. cinerea 
was 31.4 X 102 kNm 2 compared with 8.4 X 102 kNm 2 of celery cells. The 
permeability of celery cells increased at some distance from those already 
killed and in advance of the hyphae (probably as a result of pectinase activity 
on the cell walls, membranes, and protoplasm) and Thatcher considered that 
the osmotic pressure differential could explain the transfer of water and 
nutrients from the host cells to the fungus. 

The enhanced parasitism of Botrytis spp. on older, senescent or mori- 
bund tissues, for example of tomato stems infected by B. cinerea (Wilson 
1963), may probably be explained in terms of Thatcher's hypothesis, as may 
also the transition of latent infections (q.v.) in tissues of changing metabolism 
in which host-cell permeability and the relative osmotic pressure of host and 
parasite must change. 



Effects on host metabolism 

Diseases caused by Botrytis spp. are not normally wilts in the sense that 
those caused by Fusarium and Verticillium spp. are; however, Hursh (1928) 
considered that the wilt of paeony caused by B. paeoniae resulted from local 
blocking of the vessels rather than from mobile toxins, because the shoot 
remained normal if excised above the lesion and kept in water. Carranza 
(1965) ascribed the wilt symptoms caused in Cicer arietum by B. cinerea to 
necrosis of the xylem. Brierley (1918a) found that the mycelium of B. cinerea 
was confined to dead vascular elements throughout affected shoots of Ribes 
alpinum. He thought that the fungus, as it developed with the growing shoot, 
existed in a symbiotic condition with the host. 

88 



Brierley also noted that the host was stimulated to form galls and ad- 
ventitious roots. Adventitious root formation has also been noted in the 
vicinity of lesions of the stems of tomato plants infected by B. cinerea (Jarvis, 
unpublished). Wilson (1963) noticed that delaminated petioles of tomato 
inoculated with B. cinerea tended to fall from the stem earlier than non- 
inoculated petiole stubs, and Verhoeff (1967) tried to exploit this tendency 
in order to rid the plant of these stubs that were potential sites of infection 
for the whole plant. Petiole stubs about 5 cm long abscissed in about 21 
days; those inoculated at the distal end with conidia of B. cinerea abscissed 
in 8 days, often before the fungus had grown into the main stem. Ilieva 
(1971) thought a toxin was responsible for abscission. 

Lemon pedicel infection by B. cinerea was also suspected of being con- 
nected with abscission (Klotz, Calavan, and Zentmeyer 1946). Infection 
occurred at the abscission zone; although affected flowers abscissed, Klotz et 
al. were unable to determine whether the flowers abscissed before infection 
occurred or as a result of it. Beetz (1966) attributed abscission of about 10% 
of grapevine buds to the presence of B. cinerea. Skidmore and Dickinson 
(1973) could not associate the presence of B. cinerea in the phyllophane of 
barley leaves with changes in the course of senescence. 

An interesting effect on the physiology of Antirrhinum majus flowers 
infected by B. cinerea was noted by Harrison and Hopwood (1969): a 
genetically blocked anthocyanin was released to produce a distinctive color- 
ring in the corolla providing that anthocyanin production was blocked only 
by the delilah gene. 

Williamson (1950) noted that infection of Chrysanthemum tissue by 
B. cinerea resulted in the release of ethylene and Smith, Meigh, and Parker 
(1964) found that carnations infected by B. cinerea also produced consider- 
ably more ethylene; the ethylene damaged healthy flowers and predisposed 
(q.v.) them to further attack by the fungus. 



RESISTANCE 



Mechanical resistance 

Blackman and Welsford (1927) and Louis (1963) showed that the plant 
cuticle is penetrated mechanically by infection pegs of Botrytis cinerea, but 
in the field Botrytis spp. do not often seem to infect plants directly through 
the cuticle but rather from a saprophytically based mycelium. Jarvis (1962^) 
found that only about 1 % of all infections by B. cinerea of strawberry and 
raspberry fruits could be attributed to infection achieved in the manner 
described by Blackman and Welsford (1927) and Louis (1963). The re- 
mainder resulted either from development of latent infections (q.v.) from the 

89 



proximal end, equivalent to a saprophytically based mycelial infection, or 
directly from a saprophytically based inoculum adhering to or touching the 
fruit. The intact cuticle of the ripe strawberry fruit was surprisingly resistant 
to direct infection from spores. 

Ainsworth, Oyler, and Read (1938) considered the tomato fruit cuticle 
as a barrier to infection by B. cinerea in ripening fruit; the increased resis- 
tance was associated with a rather sudden change from a slightly matt surface 
to a glossy, darker-green surface as the fruit ripened. Of two different types 
of lesion, Louis (1963) attributed one, a restricted necrotic spot, to thick 
cuticles and the other, a non-necrotic spot and a non-necrotic spreading 
lesion, to thin cuticles. 

Investigating the surface of raspberry canes as a barrier to fungal in- 
fection, Jennings (1962) and Knight (1962) found the incidence of B. cinerea 
to be higher in the stems of cultivars that were relatively wax-free, hairless, 
spiny, and pigmented, and Doornik and Bergman (1971) attributed the 
resistance of tulip shoots to B. tulipae to the presence of a sheathing, brown 
scale tunic leaf. 

The intact grape cuticle is relatively resistant to B. cinerea (du Plessis 
1937; Stalder 1953^, 1955) and infection depends largely on wounds through 
the cuticle such as those caused by hail, by cracking in over-wet conditions 
or after using the wrong fungicide, and by insect punctures (Vanderwall 1937; 
Francot, Geoff roy, and Malbrunot 1956; Bessis 1972). Zilai and Lefter 
(1969) concluded that the grape cuticle was not an important barrier but they 
did find that differences in fruit susceptibility of some grape cultivars could 
be attributed to differences in the anatomy of the hypodermis, the first 11-15 
layers of cells beneath the epidermis; the thinner the layer, the greater the 
resistance to gray mold, because the layer is less liable to crack under stress 
from high water uptake by the fruit. Beukman (1963) had also found that 
resistant grape cultivars tended to have berries with thin cuticles, small epi- 
dermal and hypodermal cells, and a large ratio of radial to tangential wall 
length in the epidermis. 



Wound reactions 

Fruit cracking and bruising in cherries are usually followed by various 
fungi, including B. cinerea (Gerhardt, Enghsh, and Smith 1945: Ogawa, Bose, 
Maji, and Schreader 1972). Wet weather conditions result in cracked fruit, 
and unless the surface is dried out quickly, fungi soon invade the exposed 
parenchyma. There is no wound reaction at a storage temperature of 10°C 
but if the tissue around the crack dries out, infection is considerably reduced. 
Tompkins (1950) also found that stem cracking, resulting from excessive 
nitrogen applications, permitted the entry of B. cinerea into tuberous-rooted 
Begonia. 

90 



Wound reactions against invasion by Botrytis spp. seem relatively rare, 
probably because the fungi usually invade rapidly and kill cells in advance of 
hyphae. At 20°C wounded potato tubers are not normally parasitized by 
B. cinerea, although at lower temperatures, about 5°C, they are. Ramsey 
(1941) attributed tuber resistance at 20°C to the formation of a wound 
periderm, but it was inadequate if tubers were transferred to 5°C within 
3 days and then inoculated. 

A periderm was also noted by Bald (1953^, 1953^) in Gladiolus corms 
and its formation too was related to temperature. B. gladioUorum has an 
optimum temperature for growth in vitro of about 20° C but, because this 
temperature also favors periderm formation, parasitism is considerably re- 
duced. Bald found that curing the corms at 35 °C immediately after digging 
promoted the formation of periderm. 

Bald (1953fl) also attributed resistance in Gladiolus leaves to the forma- 
tion of gum as well as to cuticle thickness in both leaves and corms. 

The formation of gum-like material in lettuce leaves in response to in- 
fection by B. cinerea was reported by Abdel-Salem (1934). The formation 
occurred in cells with thick brown walls adjacent to a zone of healthy cells 
bounding infected areas. Brown and Montgomery (1948), howeveY, could 
find no abscission layer formed as a defence reaction in affected lettuce leaves, 
but Zeller (1926) found that in pear flowers the spread of B. cinerea through 
the pedicel was checked by the normal abscission layer at its base. In con- 
trast, strawberry and raspberry receptacles are not shed, as pear fruits are, 
and the fungus is able to spread from fruit to fruit along pedicels (Jarvis, 
unpublished). 

Cartel (1965^, 1965^) found that B. cinerea could be excluded by callus 
tissue if woody tissues of grapevine were stored at 25-30°C after grafting but 
the fungus was able to infect the material at 15°C because callus formation 
was negligible at lower temperatures. The fungus grew well at 15°C and even 
at 3°C it grew at 0.1 mm/h; its growth was checked at 28-30°C but it was 
not killed. 



IMMUNITY 

Beginning with Nobecourt (1928), many investigators thought that pre- 
treating plants with various filtrates from cultures of Botrytis cinerea rendered 
the plants more resistant to subsequent inoculation with the fungus; the 
investigators include Carbone (1929), Carbone and Jarach (1931), Baldacci 
(1932), Jarach (1932), Carbone and Kalyayev (1932), Kalyayev, Kravtchen- 
ko, and Smirnova (1935), Carbone and Arata (1934), and Arata (1935). 
However, Baldacci (1935) and Carbone (1935) discounted the hypothesis 
of immunity acquired in this way and so did Butler (1936). The idea was 
finally quashed by Baldacci (1937) and by Baldacci and Cabrini (1939) who 
showed that the fungus used in much of the earlier work was not B. cinerea, 

91 



but a species of Rhizoctonia (Corticium vagum var. amhiguum), the causal 
organism of the 'toile' disease of beans. 

Heale and Stringer-Calvert (1974), re-opening this type of work, treated 
carrot callus tissue cultures with fluid in which spores of B. cinerea had 
germinated. Four days later, Heale and Stringer-Calvert inoculated the tissue 
with spores; symptoms were delayed 1-7 days in comparison with those on 
the check tissue, and the onset of symptoms was associated with increasing 
levels of insoluble invertase activity in the tissue. 



Chemical resistance 

The cuticle, in addition to the offering possible mechanical resistance to 
infection, has some components that are fungistatic. Jarvis (unpublished) 
found that acidic fractions of the cuticular wax of Rubus idaeus and R. 
phoenicolasus, in comparison with other fractions, retard the growth of B. 
cinerea when incorporated into agar. Schlitt {\91\a) found that different 
components of conifer needle wax had different effects on the growth of 
B. cinerea but the effects differed with host species and fungal isolate, and 
resistance could not be interpreted in terms of chemical resistance at the 
cuticle. Blakeman and Sztejnberg (1973) found that germination of conidia of 
B. cinerea was inhibited by the surface wax of beetroot leaves. 

Topps and Wain (1957) found that exudates washed from the leaves of 
some plants were inhibitory to the spores of B. cinerea, especially exudates 
from Sambucus nigra and Ligustrum vulgare. Topps and Wain suggested 
that exudates, concentrated on the leaf surface, could play some part in 
resistance. 

Beneath the cuticle many plant tissues have intrinsic resistance to the 
growth of Botrytis spp. and there have been some attempts to correlate re- 
sistance with the growth of the fungi in various tissue extracts (e.g., Irvine and 
Fulton 1959). However, such extracts are notoriously difficult to prepare 
without altering their components and results must be treated with caution. 
Even the growth of hyphae through tissue is usually a poor measure of re- 
sistance or susceptibility because it takes into account only one factor among 
many and it is difficult to associate with any particular chemical or mecha- 
nism. For example, Stalder (19536) considered that the resistance of berries 
of different grape cultivars to the growth of B. cinerea was not connected with 
the mechanical properties of the host tissue, nor with any induced reaction, 
but with the chemical composition of the cell sap. However, he could find no 
correlation between fungal growth rate and sugar, acid content, or pH. 

Only a few relatively simple materials have been implicated, directly and 
unchanged, ifi resistance. Nobecourt (1927) considered leaves of Prunus 
laurocerasus to be resistant to B. cinerea because of the presence of benzoic 
aldehyde and Fijikawa and Miyazaki (1960) found astringent cultivars of 
persimmon, because of their higher tannin content, more resistant than sweet 

92 



cultivars. On the other hand Vanev (1965) found tannins from grapevines 
had no adverse effect on the germination and growth of B. cinerea in vitro. 
Polyphenols are normally considered to impart resistance in many diseases 
(Kosuge 1969) but Orellana and Thomas (1965) thought that the gallic acid in 
Ricinus communis could well account for the specificity of B. ricini to this 
host. The fungus grew well in 0.4% gallic acid, spores germinated better in 
0.1% than in water, and sporulation was abundant on media containing be- 
tween 0.01 and 0.1% gallic acid. 

Sokolov, Chekhova, Eliseev, Nilov, and Shcherbanovskii (1972) found 
juglone to inhibit the growth of B. cinerea at a concentration of 2 f<.g/ml, and 
the related plumbagin and 1,4-naphthoquinone inhibited at 10 /xg/ml. 

Martin (1973) reported that some furanocoumarins (pimpinellin, iso- 
pimpinellin, bergapten, and sphondylin) from Heracleum sphondylium sup- 
pressed the mycelial growth of B. cinerea at about 500 ppm. 

Spencer, Topps, and Wain (1957) found a material in the lower stem 
and upper root tissues of Vicia faba that inhibited the germination of spores 
of B. cinerea and of B. fabae. The fungistat was believed to be phenolic and 
reducing. 

A number of fungistatic materials, known as phytoncides, have been 
extracted from various plants, especially from Brassicae and Allium spp. 
Marchevskaya (1955) and Vanev (1969) extracted phytoncides from Armo- 
racia rustica, Allium sativum, Brassica napus, Raphanus sativus, and Nastur- 
tium officinale, which were inhibitory or stimulatory to Botrytis cinerea in 
vitro, depending on their concentration. 

A series of investigations by Walker and his colleagues showed that 
materials in colored onion cultivars imparted resistance to some fungi but 
others in white cultivars imparted resistance to different fungi. Walker and 
Lindegren (1924) found that the neck-rot organism, B. allii (B. aclada), could 
attack the fleshy scale leaves in bulbs of colored cultivars only when the 
colored scales were circumvented through wounds. Walker, Lindegren, and 
Bachmann (1925) recognized two types of inhibition, one from a thermostable 
toxin and the other from volatile materials; and Walker and Link (1935) 
considered these results in terms of a phenolic resistance mechanism. Al- 
though phenol, catechol, and salicylic acid retarded growth of B. allii, com- 
parable concentrations of guaiacol, veratric acid, vanillic acid, and proto- 
catechuic aldehyde stimulated growth. Walker and Link concluded, however, 
that the inhibitory compounds played no significant part in defence because 
of their low concentration and location in the tissues. Walker, Morell, and 
Foster (1937) found B. allii only slightly sensitive to the vapor phase of 
mustard oils; the allyl mustard was very toxic, but not as toxic as its glycoside, 
sinigrin, the form in which it usually occurs in the unwounded plant. Hatfield, 
Walker, and Owen (1948) found B. allii less sensitive to the nonvolatile than 
to the volatile materials of succulent scale leaves. When B. allii gained access 
to the fleshy scales, there was no correlation between resistance and the color 
of the outer scales, but resistance was correlated with pungency and with the 

93 



toxicity of volatile and nonvolatile substances in the fleshy scales. Walker, 
Owen, and Stahmann (1950) concluded that the volatile sulphides were prob- 
ably responsible, and so, to a lesser extent, were the phenolic materials. 
Bergquist and Lorbeer (1971) found the sclerotia of B. squamosa more nu- 
merous on the neck of cultivars with white bulbs and those with yellow bulbs 
than on the neck of cultivars with bulbs of other colors. 

The role of phenolic compounds has been implicated in many resistance 
mechanisms, for example in the resistance of grape berries to B. cinerea 
(Pliskanovskii and Zotov 1971; Pliskanovskii 1972; Zotov and Pliskanovskii 
1973; and Rizvanov and Karadimcheva 1973) but their role is usually very 
complex. Free polyphenols, which are phytotoxic, probably rarely exist as 
such in plants, but rather in combination with sugars as glycosides, which may 
be stimulatory to fungi (Talieva 1954; Sproston 1957). 

The complex role of polyphenolic and other systems, particularly in 
cabbage infected by B. cinerea, has been extensively investigated by Rubin and 
his colleagues and reviewed by Rubin and Ivanova (1960) and Rubin and 
Artsikhovskaya (1963, 1967). 

When cabbage head leaves were infected by B. cinerea, peroxidase activ- 
ity increased considerably, some other enzyme systems were inhibited (Rubin 
and Chetverikova 1955), and respiratory activity was intensified around the 
infection site (Rubin, Chetverikova, and Artsikhovskaya 1955). There was 
4-5 times as much readily oxidizable amino acid content in the resistant cul- 
tivar Amager as in the susceptible cultivar No. 1 ; infection resulted in greatly 
increased ascorbic acid oxidase activity in the resistant but not in the suscep- 
tible cultivar (Rubin and Ivanova 1958, 1959). Rubin, Ivanova, and Davy- 
dova (1961) and Rubin and Ivanova (1963) attributed the darkening of in- 
fected tissues of the resistant cultivar Amager to the accumulation of fungi- 
static water-soluble tannins and free polyphenols. Precursors of these mate- 
rials (phloroglucinol, caflfeic, and chlorogenic acids) were presumed to be 
oxidized by polyphenol oxidase secreted by B. cinerea because the enzyme 
is absent from healthy cabbage. Ivanova, Davydova, and Rubin (1965) also 
found vanillin and another unidentified phenol in cabbage to be toxic to B. 
cinerea. The oxidation products affect the activity of the fungal dehydroge- 
nases (Ivanova and Rubin 1963; Rubin, Ivanova, and Davydova 1964/?). 

The resistant cabbage cultivar Amager had a higher peroxidase activity 
than cultivar No. 1 (Rubin, Artsikhovskaya, and Spiridonova 1939) and the 
activity was considerably enhanced when infection occurred; Rubin, Ivanova, 
and Davydova (1964g, 1965) considered that the enhanced activity would 
contribute to resistance. The increase in activity was the result of enzyme 
synthesis (Rubin, Aksenova, and Kozhanova 1973). Aksenova, Ksivan'ski, 
and Rubin (1966) also found that NADH-cytochrome-C-reductase, as a 
component of the respiratory system, plays an important part in the defence 
reaction. Protein synthesis is another feature in parasitized cabbage tissue 
(Rubin, Aksenova, and Nguyen Din Guen \91\a, \91\b\ Rubin, Aksenova, 
and Brynza 1973) and occurs in mitochondria (Rubin 1973«, 19736). 

94 



Brynza and Aksenova (1973, 1974) found that mitochondria from re- 
sistant cabbage infected by B. cinerea had higher values for RC (respiratory 
control) and ADPiOo ratio than those from healthy tissues. The mitochon- 
drial membranes were damaged during infection in the susceptible cultivar 
and coupling in oxidative phosphorylation decreased; respiratory control had 
been lost. 

Some of these results have been exploited in breeding programs by 
Brumshtejn and Metlickij (1963); in seeking new cabbage cultivars with re- 
sistance to B. cinerea, they selected seedlings showings high peroxidase 
activity. 

The failure of B. cinerea or of pectinases extracted from it to attack 
tissues with a high polyphenoloxidase activity has long been of interest. Chona 
(1932), trying to explain the apparent resistance of potato tissue, found that 
the enzymes were inactivated by potato juice, but attributed this to the action 
of certain salts, particularly magnesium sulphate and potassium phosphate. 
Folsom (1933) noted that when B. cinerea attacked potato tubers, the lesion 
was sometimes restricted by darkened tissue. Trzebinski (1962) found a similar 
situation in sugar-beet roots attacked by B. cinerea; those cultivars having 
a strong polyphenoloxidase reaction were resistant, and those with non-brown- 
ing tissues were not. Although B. cinerea is able to rot apples slowly (Cole 
and Wood 1961), oxidized apple juice rapidly inactivated the pectinase en- 
zymes of an isolate from apple, but not those of an isolate from lettuce 
(Cole 1956). 

Deverall and Wood (1961^) found that both B. cinerea and B. fabae 
produced pectinases and cellulases capable of macerating tissue of Vicia faba, 
although in the quiescent (q.v.) phase of the chocolate spot disease there is 
little evidence of tissue breakdown. They also found that products of phenolic 
oxidation inhibit pectinases, but products of pectin degradation activate latent 
polyphenoloxidase. They proposed a hypothesis with the following sequence 
of events: the fungus infects the tissue and begins to secrete cell- wall- 
degrading enzymes; the degradation products in turn promote the secretion of 
more enzymes and also provide nutrients for the pathogen. The products of 
cell-wall degradation also activate the latent polyphenoloxidase system of the 
moribund host cells; it then acts on phenols released on cell death. The re- 
sultant oxidized phenols inhibit pectinase activity and so the lesion is res- 
tricted. In the aggressive phase of chocolate spot, B. fabae spreads rapidly 
through the tissue; it was suggested that conditions of changing host metabo- 
lism permit the fungus to produce cell-wall-degrading enzymes faster than 
they can be inactivated. A similar hypothesis seems to hold for the resistance 
of young tomato stem tissue to infection by B. cinerea (Jarvis and Wilson, 
unpublished). 

Young tomato-stem tissues, compared with old tissues, are more resis- 
tant both to the growth of B. cinerea through them and to the germination 
of conidia in their vessels; germination is inhibited in the latent phase of the 
disease (see PART 4, "Latency"; also Jarvis and Wilson, unpublished). If 
conidia lie ungerminated in a vessel, local browning — apparently phenolic 

95 



in nature — occurs in the cell wall. Young tissue had a generally higher 
polyphenoloxidase activity, depending on the enzyme substrate, than old tis- 
sue and the activity was not increased by activators of latent polyphenoloxi- 
dase; old, susceptible tissue had a low polyphenoloxidase activity, which was 
increased by activators of the latent enzyme. Although these results do not 
seem entirely compatible with the Deverall and Wood hypothesis, the results 
can be explained in terms of pectinase inhibition: young, resistant tissue, with 
a very active polyphenoloxidase system, inhibits pectinase activity; old tissue, 
because of the low, non-activated state of its polyphenoloxidase system, does 
not. 

Thomas and Orellana (19636) could not relate the resistance of capsules 
of some cultivars of castor bean to their phenolic content (indeed B. ricini 
can tolerate relatively high concentrations), but in a subsequent paper (1964) 
they associated resistance with the inactivation of fungal enzymes by means 
of oxidation products of phenols from damaged host-cells. Capsules of re- 
sistant cultivars had a relatively low content of flavanols and related com- 
pounds, and significantly more active peroxidase and polyphenoloxidase 
systems. 

On the basis of these findings, Thomas and Orellana (19636) devised two 
simple biochemical tests for susceptibility. In one, they sprayed capsules with 
a commercial pectinase preparation; after incubation, susceptible capsules 
became brown and macerated while resistant capsules remained green and 
firm. In the other test, crushed tissue was treated with reagents (ferric chlo- 
ride, vanillin-sulfuric acid, or potassium ferri cyanide) for oxidized phenols; 
a positive color reaction indicated resistance. Esuroso (1969) used the pec- 
tinase test to screen potential cultivars for Nigerian conditions and according 
to test results, no cultivar was considered suitable. 

Sproston (1957) investigated the role of glycosides in the resistance of 
Impatiens balsamina using as a test fungus B. allii (B. aclada), which is not 
normally a parasite of this host. Conidia germinated on the leaves and 
penetrated them but a dark-color reaction occurred and no further growth 
took place. Kaempferol, quercetin, and 2,3-dimethoxy-2-methoxy-l,4-naph- 
thoquinone were isolated from the affected tissues. Sproston considered them 
too phytotoxic to exist as such in the healthy plant and thought that they 
probably occur as glycosides that are broken down in the host-parasite com- 
bination to release the fungitoxic phenolic moiety, which may then be 
oxidized. 

Sokolov, Chekhova, Eliseev, Nilov, and Shcherbanovskii (1972) found 
1 ,4-naphthoquinone to be lethal to B. cinerea at 10 /xg/litre and the related 
juglone and plumbagin at 2 ^g/litre and 10 /xg/litre. 

Schmitt (1952) found that a defence reaction of seedlings of Lepidium 
sativum to B. cinerea, the deposition of melanic pigments on cell walls and 
the development of a cortical cambium, was enhanced in high light intensities, 
but not in low intensities. 

96 



The ultrastructure of the B. fabae — Vicia faba relationship was in- 
vestigated by Abu-Zinada, Cobb, and Boulter (1973). They found that the 
cytoplasm of invading hyphae was slightly less dense than that of external 
hyphae and that at the interface there were lomosome-like structures in the 
fungus, perhaps the sites of hydrolytic enzyme production. At the periphery 
of the lesion, host cells contained large volumes of cytoplasm, numerous Golgi 
bodies, and a well-developed endoplasmic reticulum. Host cells also contained 
various unidentified bodies and inclusions, and Abu-Zinada et al. suggested 
that unidentified electron-dense bodies in the extracellular spaces of the host 
might be remnants of fungal mycelium acted upon by enzymes of the host. 
Incubating mycelium in an extract of bean leaves infected by B. fabae resulted 
in considerable disorganization of fungal fine structure. 

The resistance to B. cinerea of flowers of Paeonia spp.. Primula sinensis, 
Forsythia europaea, F. suspensa, Gentiana lutea, and Antirrhinum majus was 
investigated by Jung (1956) and Schonbeck (1968). In no case was the ovary 
entered; stigma secretions enhanced spore germination, but growth was 
halted in the style, which remained turgid long after other flower parts had 
withered. The resistance of the style was unaffected by changes in temperature 
or light, by its age, or by wounds. A fungal inhibitor, which enhanced pollen 
tube growth, was present in the stigmas and styles; it was water-soluble and 
destroyed by ultraviolet light and exposure to 60 °C. lost, Volken, and Kern 
(1964) suggested that an inhibitor found in the stigma and style of Trifolium 
pratense accounted for the failure of B. anthophila to attack female parts of 
the flower. 

Schonbeck (1966) found a principle in the stigma of Tulipa that inhibited 
the growth of B. cinerea but stimulated that of B. tulipae, its normal pathogen. 
The concentration of the active principle was low in stamens, bulb, and roots, 
but high in petals and very high in green leaves. It was probably a-methylene 
butyrolactone (Bergman and Beijersbergen 1968). 

Later, Schroeder and Schonbeck (1970), Schroeder (1972<3), and Schon- 
beck and Schroeder (1972) attributed resistance to the presence of tuliposides 
(1-acylglycosides) that were released by the pistil because of increased cell 
permeability caused by B. cinerea and, to a lesser extent, by B. tulipae. Under 
the influence of B. cinerea, the tuliposides became degraded to lactones with 
a high antibiotic activity, whereas under the influence of B. tulipae, acids with 
a low activity were formed. 

Schroeder (1972Z?, 1972c) further showed that B. cinerea and B. tulipae 
differed in their production of pectinases and of citric and oxalic acids. 

In Cyclamen persicum, Schlosser (1971, 1973) showed that the saponin 
cyclamin, which B. cinerea cannot detoxify, could be responsible for the 
resistance of leaves. The concentration of cyclamin in stems, however, was 
considered low enough to permit their parasitism. 

Arneson and Durbin (1968) investigated the role of the glyco-alkaloid 
a-tomatine in resistance of tomato to various fungi. In general, non-tomato 

97 



pathogens were more sensitive in vitro to a-tomatine than tomato pathogens; 
B. cinerea, a pathogen of tomatoes, was inhibited at 0.013 M. Arneson and 
Durbin concluded that a-tomatine was present in leaves at toxic concentra- 
tions (about 10~3 M), but it was localized in tissues and intracellular sites and 
could be avoided by some fungi. Verhoeff (personal communication) con- 
sidered that B. cinerea could detoxify a-tomatine, so this substance was prob- 
ably unimportant in resistance to the fungus. 

Brown (1915) and Nelson (1956) had suggested that some resistance 
might be associated with the chemical and/or physical states of pectic mate- 
rials in cell walls, and Hondelmann (1969) and Hondelmann and Richter 
(1973) attributed the relative resistance of fruit of certain strawberry cultivars 
to a low ratio of soluble to insoluble pectin. Those berries with a high ratio 
were less firm and more susceptible to B. cinerea. 

This ratio is possibly influenced by the calcium content of the fruit. 
Indeed Silvestrov (1961) was able to reduce by about 90% the incidence of 
gray mold in strawberries by liming the plantation at a rate of 800-900 kg/ha 
(about 15-20 g/plant), although this result may have other explanations based 
on altered pH values in soil and altered metabolism in the host or in the para- 
site. Similarly, Stall (1963) and Stall, Hortenstine, and Iley (1965) reduced 
the incidence of gray mold in tomatoes; a lower content of phosphorus in the 
tissue also contributed to resistance. Tissue with a high Ca and a high P 
content was as susceptible as that with a lower Ca and lower P content. Again, 
Krauss (1971) found that lettuce plants with an increased Ca content had 
increased resistance to gray mold. When he found that high levels of nitrogen 
increased growth and decreased resistance, he suggested that the Ca level in 
the plant had been relatively decreased. He further suggested that the ob- 
served resistance of P- and N-deficient plants was the result of their relatively 
high Ca content and smaller cells. In plants with adequate Ca, the incidence 
of the disease was less affected by anion concentrations, the pectin was less 
soluble, and the cell membranes were less permeable. 

Francot, Geoffroy, and Malbrunot (1956) and Bolay, Bovay, Neury, and 
Simon (1967) reported Ca-induced resistance to B. cinerea in grapes. 

Deverall and Wood (1961^) found Ca-deficient bean plants more sus- 
ceptible to B. fabae and suggested that their cell walls were more easily 
penetrated and degraded by the fungus. Similarly, Thomas and Orellana 
(1963ft, 1964) attributed the resistance of capsules of some castor-bean culti- 
vars attacked by B. ricini to a relatively high content of insoluble pectin and 
high contents of calcium and magnesium, both of which contribute to pectin 
insolubility (Joslyn 1962). 

Other physical changes occur in infected tissues and there are differences 
between susceptible and resistant tissues. Rubin and Sipilov (1963) detected 
wide differences in the electrical potential difference from the external envi- 
ronment to cell contents between resistant and susceptible cabbage tissues 

98 



and between tissues infected by B. cinerea and those not infected. Aksenova 
and Savchenko (1966) found the permeability of protoplasm in resistant 
cabbage tissue to be increased by 12% on infection by B. cinerea and by 
120% in a susceptible cultivar. Infection resulted in the displacement of the 
isoelectric point. It also resulted in an increase in mitochondrial size and in 
ribosome number in the susceptible cultivar No. 1, but not in the resistant 
cultivar Amager (Rubin, Aksenova, and Nguyen Din Guen 19716). Although 
enhanced protein synthesis was associated with ribosomes in infected Amager 
and with mitochondria (Rubin 19736), there was protein degradation in in- 
fected No. 1 (Aksenova, Rubin, Savchenko, and Brynza 1968; Rubin, Akse- 
nova, and Nguyen Din Guen 197 la, 19716; and Rubin, Aksenova and 
Kozhanova 1973). 

Aksenova and Savchenko (1965) found that in the resistant cultivar 
Amager, energy-storing processes were retarded immediately around an 
inoculum of B. cinerea, and the intensity of oxidative phosphorylation in- 
creased just outside the inoculation zone. In the susceptible cultivar No. 1, 
energy storage remained unaltered near the inoculum, and in the surrounding 
zone phosphorylation increased at first, then decreased. 

Other biochemical differences m mtected tissues of resistant and suscep- 
tible cabbage cultivars were noted by Ozereckovskaya and Voronkov (1964), 
in tissues both at the site of infection and at some distance from it. In suscep- 
tible tissues, oxygen absorption was stimulated by 2,4-dinitrophenol, the con- 
tent of inorganic phosphate decreased, and that of alcohol increased. 

The overall nutrition of plants is important in determining their resis- 
tance as well as their predisposition (q.v.). Home and Gregory (1928) asso- 
ciated the resistance to B. cinerea of the fruit of some apple cultivars to a low 
water content, high acidity, a high K content, and a low N content. Colhoun 
(1962) lowered the resistance of apple fruit by injecting urea and potassium 
phosphate into the branch; both materials together were more effective than 
either alone. 

Verhoeff (1965) examined the effects of N, P, K, Mg, and lime as soil 
amendments on the extension of lesions caused by B. cinerea on tomato stems 
and petioles, and on the rate of mycelial growth through the tissues. Higher 
levels of soil N resulted in slower rates of lesion extension, especially on 
stems, and in slower rates of mycelial growth. For a given level of soil N, 
higher rates of K decreased the rates of lesion development; the N:K ratio was 
therefore important. Lesions developed more rapidly near the shoot apices. 
These effects were also demonstrated under commercial conditions (Verhoeff 
1968). 

In strawberry, the correct use of maganese, copper, and boron as trace- 
element fertilizers reduced the incidence of B. cinerea in the fruit (Dorozhkin 
and Grishanovii 1972). 

99 



Phytoalexins 

A phytoalexin, a substance formed or activated only in the host-parasite 
combination (Deverall 1972), was recognized first by Purkayastha and De- 
verall (19646, 1965) in a disease caused by a Botrytis sp. Diffusates from 
leaves of Vicia faba, infected by B. cinerea, contained substances that in- 
hibited the germination and germ tube growth of both B. cinerea and B. fabae. 
Relatively less antifungal material was present in diffusates from lesions 
caused by B. fabae. 

Infection drops in bean-pod cavities and containing spores of B. cinerea 
became inhibitory to the growth of germ tubes within 18 h (Deverall 1967). 
The inhibitor, which was ether-soluble, counteracted the stimulant effects of 
sucrose, glucose, fructose, galacturonic acid, or several amino acids that were 
also present in the drops. Drops containing spores of B. fabae contained 
relatively large amounts of a UV-absorbing, biologically inactive substance. 

Deverall, Smith, and Makris (1968) also found a phytoalexin in diffusates 
from lesions in pods of Vicia faba and Phaseolus vulgaris if the lesions were 
caused by B. cinerea. An inhibitor was also found in diffusates from the larger 
lesions caused by B, fabae and it was concluded that B. fabae was able to 
detoxify the inhibitor. Deverall and Vessey (1969) found that the phytoalexin 
in V. faba was an ether-soluble acid formed by apparently healthy cells in 
advance of hyphae of B. fabae or B. cinerea and also in response to physical 
injury. Deverall and Vessey thought that the greater ability of B. fabae to 
detoxify the phytoalexin could explain its greater pathogenicity in the aggres- 
sive phase of the bean chocolate-spot disease, and similarly that B. cinerea, 
because of its poor abiUty to detoxify the phytoalexin, had relatively poor 
pathogenicity on bean (Deverall and Wood \96\a). 

The phytoalexin was characterized and named wyerone acid by Letcher, 
Widdowson, Deverall, and Mansfield (1970) and Fawcett, Firn, and Spencer 
(1971). The biosynthesis of wyerone acid in the host was greatly stimulated 
by the presence of the pathogen, and the phytoalexin reached a maximum 
concentration 4 days after inoculation; it then appeared to be metabolized 
— possibly to wyerone, an antifungal ester, which had been found in healthy 
seedlings of V. faba by Fawcett, Spencer, and Wain (1969). Balasubramani, 
Deverall, and Murphy (1971) noted high respiratory activity in parasitized 
leaf discs, which, they thought, might reflect inhibitor production. High poly- 
galacturonase activity also occurred in and around lesions despite the pres- 
ence of a polyphenoloxidase system known to be inhibitory in vitro (Deverall 
and Wood 19616). 

Further work on the detoxification of wyerone acid was done by Mans- 
field and Widdowson (1973). B. fabae reduced wyerone acid, both in vitro 
and in infection droplets in bean-pod cavities 1-3 days after inoculation. 
Though wyerone acid was metabolized by B. cinerea slowly in vitro, reduced 
wyerone acid could not be detected. Mansfield, Porter, and Widdowson (1973) 
identified the B. fabae metabolite of wyerone acid as 3-[5-(hyaroxy-d5'-hept- 

100 



4-enyl)-2-furyl]-rraAT5-prop-2-enoic acid, which compares with CH3CH2CH = 
cue ^ ceo (C4H2O) CH = CHCOOR, where R is H, CH3 for wyerone 
acid and wyerone, respectively. 

Whereas Mansfield and Deverall (1974^) thought that wyerone acid 
production was confined to dying cells in lesions, Mansfield, Hargreaves, and 
Boyle (1974) suggested that it was also formed in individual, but not all, living 
cells in lesions caused by B. cinerea. They thought that phytoalexin produc- 
tion could be triggered initially by cell death in response to fungal invasion 
or that metabolites released from dead cells might induce synthesis of wye- 
rone acid in adjacent living cells. Another possibility was that fungal metab- 
olites might act as specific inducers of phytoalexin production in live cells; 
wyerone acid might then reach phytotoxic concentrations in some host cells. 

Attempting to explain the pollen-induced enhancement of infection, 
Deverall and Rogers (1972) found that pollen diffusates were pH-dependent 
and that they considerably reduced the antifungal activity of wyerone acid, 
as did some other components of natural media. 

In 1974 Mansfield and his students (personal communication) found 
three other fungal inhibitors accumulating in bean tissues after inoculation 
with B. cinerea. 

Another phytoalexin, lyubimin, was formed in potato in response to 
infection by B. cinerea (Metliskii, Ozeretskovskaya, Chalova, Vasyukova, and 
Davydova 1971), and yet another in Ginkgo biloba (Christensen and Sproston 
1972). 

Cruikshank and Perrin (1963), studying phytoalexin production in pea 
pods inoculated with various fungi, found that B. allii (B. aclada), not a pea 
pathogen, induced the formation of pisatin in sufficient amount to inhibit 
fungal growth. B. cinerea, a wound pathogen, induced the formation of some- 
what more pisatin and was moderately inhibited by it. Normal pea pathogens 
were not inhibited. 

In fruits of Capsicum frutescens, inoculation by non-pathogenic fungi 
induced the formation of a sesquiterpene, capsidiol (Stoessl, Unwin, and Ward 
1972; Gordon, Stoessl, and Stothers 1973; and Ward 1973), but B. cinerea, 
a pathogen of pepper, induced only small amounts. B. cinerea was apparently 
able to detoxify capsidiol by oxidation, first to a ketone, capsenone, then to 
other undetermined compounds (Ward and Stoessl 1972^, 1972^; Stoessl, 
Unwin, and Ward 1973). 

There are many resistance mechanisms against Botrytis spp. and no single 
chemical or physical resistance mechanism can be considered general. The 
host-parasite combination must be regarded as a complex entity with interac- 
tions between many enzyme systems in host and parasite; some of these in- 
teractions are significant in the direct restriction of the fungus. 

101 



QUIESCENT INFECTIONS 



Many Botrytis diseases are characterized by a period of varying or in- 
definite duration when the fungus is apparently inactive in a symptomless host 
(latent) or when a lesion is visible but not extending (nonaggressive, as op- 
posed to aggressive when lesions are expanding). The latter terms were 
apparently first used by Beaumont, Dillon Weston, and Wallace (1936) to 
describe leaf and petal spots in tulip caused by Botrytis tulipae; the terms 
were later applied by Wilson (1937) to the chocolate spot disease of Vicia 
faba caused by B. cinerea (sic, = B. jahae) and by Brooks (1939) to rose 
petal spotting caused by B. cinerea. 

The terms aggressive and nonaggressive, although descriptive in this 
context, are unfortunately liable to be confused with the term aggressive that 
is used by van der Plank (1968) to denote pathogenicity operating against 
oligo- and polygenic resistance. 

Although latent and quiescent infections by Botrytis spp. have not always 
been recognized as such, they appear relatively common and include the 
following: 



B, cinerea: 

strawberry and rye leaves 
potato leaves 
strawberry flowers 



raspberry flowers 
black currant flowers 

grape flowers 



Macadamia flowers 

eggplant flowers 
apple flowers 



Kerling (1964) 

Holloman(1967) 

Rose (1926), Powelson (1960), 
Jarvis (1962«), Jarvis and Bo- 
recka (1968),Schonbeck (1967^), 
and Borecka, Bielenin, and Rud- 
nicki(1969) 

Jarvis (1962«) 

Bennett and Corke (1973), Jarvis 
(unpublished) 

Natal'ina and Svetov (1972&), 
Parle and Dodanis (1973), Mc- 
Clellan (1972), McClellan and 
Hewitt (1973), and McClellan, 
Hewitt, La Vine and Kissler 
(1973) 

Holtzmann (1963) and Hunter, 
Rohrbach, and Kunimoto (1972) 

Marras and Corda (1970) 

Edney (1964), Bondoux (1967), 
and Olivier and Bondoux (1970, 
1972) 



102 



pear flowers 

globe artichoke in storage 

tomato fruit, ghost spot 



onion 

sunflower seedlings 

vascular system of Ribes alpinum 

vascular system of tomato 

petals generally 
Cyclamen petals 
rose petals 

Chrysanthemum petals 

B.fabae: 

leaves of Vicia faba 



B, allii: 

onion leaves 

B. elliptica: 

rosette leaves of Lilium candidum 

B, convoluta: 

Iris rhizomes 

B, tulipae: 

tulip petals and leaves 



B, narcissicola: 

Narcissus petals and bulbs 

It seems likely that most petal 
nonaggressive infection. 



Mezzetti and Pratella (1961) 

Link, Ramsey, and Bailey (1924) 

Read (1936), Ainsworth, Oyler, 
and Read (1938), Darby (1955), 
Owen and Ferrer (1957), Ferrer 
and Owen (1959), Verhoeff 
(1970), and Kishi, Albuquerque, 
and Yumoto (1972) 

Clark and Lorbeer( 1973a, 1973/?) 

Tircomnicu and lescu (1973) 

Brierley (1918a) 

Wilson (1963), and Verhoeff 
(1965, 1967, 1968) 

Trojan (1958) 

Wenzl (1938a) 

Brooks (1939), and Wenzl 
(19386) 

Taylor and Muskett (1959) 

Wilson (1937), Yu (1945), Bre- 
mer (1954), and Sirry, Ashour, 
and Hegazi (1966) 

Elarosi, Michail, and Abd-el- 
Rehim (1965) 

Cotton (1933), Taylor (1934) 

Maas and Powelson (1970) 

Beaumont, Dillon Weston, and 
Wallace (1936), and Price (1967, 
1970) 

Jarvis (unpublished) 
flecking by any species of Botrytis is 



The factors determining whether visible lesions are of the aggressive or 
nonaggressive type have been examined only in few cases. In the bean choco- 
late spot disease, Wilson (1937) found that aggressive lesions were formed 
only when a sufficiently large concentration of spores was used in the inocu- 

103 



lum, and when the plants were kept in a high relative humidity to maintain the 
necessary water film around the spores for some days, at a temperature be- 
tween 15°C and 20°C. Wastie (1962) thought that if the primary lesions, each 
caused by penetration from a single spore, were widely spaced on the leaf, 
the host defence mechanism prevented their further development, but if 
lesions were sufficiently close together, at some critical degree of crowding, 
apparently some synergistic effect between lesions overcame resistance. 

Leach (1955) investigated the chocolate spot disease of beans again. 
Although Wilson (1937) had been confident that B. cinerea was the cause of 
the disease in East Anglia, Ogilvie and Munro (1947) had ascribed it to B. 
fabae in the west of England. Leach found that leaf spots caused by B. cinerea 
were inconspicuous compared with those caused by B. fabae and frequently 
B. cinerea affected only the epidermal cells (reminiscent of ghost spot in 
tomato), whereas B. fabae caused necrosis deep into the mesophyll. Leach 
considered aggressive infection to result from one or more of four conditions: 
(i) the infection of tissue damaged by frost, hail, insects, etc.: (ii) very heavy 
leaf spotting; (iii) infected flowers and moribund and dead flowers lying on 
leaves; and (iv) the senescence of lightly spotted leaves. Dead flowers were 
almost always infected only by B. cinerea, and B. fabae appeared on them 
only when it was sporing profusely on the lower (senescent) leaves as the 
epidemic progressed. Thus, any environmental factors leading to premature 
senescence, such as poor soil drainage or deficiency of potassium or phospho- 
rus, would also lead to aggressive leaf infection, the epidemic phase of the 
disease. 

B. cinerea is usually a nonaggressive pathogen on leaves of Vicia faba, 
but B. fabae causes spreading lesions; this situation has been studied by Wastie 
(1962), Deverall and Wood (1961^), Purkayastha and Deverall (1964^, 
1965), Purkayastha (1966), Deverall, Smith, and Makris (1968), Deverall 
and Vessey (1969), and Abu-Zinada, Cobb, and Boulter (1973) in the terms 
of infectivity and resistance mechanisms, and is more fully described in the 
PART 4, "Resistance". 

Price (1967, 1970) found that a high concentration of spores of B. tuli- 
pae, such as could be provided by rain-splashed spores, was required in the 
inoculum to give an aggressive lesion on tulip leaves, and that prolonged 
humid conditions were also required. In humid conditions, nonaggressive 
lesions became water-soaked but rarely enlarged. They were mostly confined 
to the upper leaf surface and were more numerous if the wax was removed 
from the leaf before inoculation. 



Latency 

As defined by van der Plank (1968), the latent period is the time needed 
for a generation of a pathogen, that is, the period from the arrival of infective 
propagules at the host surface until the new pathogen colony becomes a 
source of infection. By contrast, the time needed for symptoms to appear is 
the incubation period. 

104 



Because tissues newly infected by Botrytis cinerea act as an effective 
inoculum, latency may be quite short (sensu van der Plank 1968), but the 
incubation period, and the latent period, as defined by the appearance of 
conidia on lesions, may be quite long and have important implications in the 
design of control measures. 

Powelson (1960) demonstrated the presence of B. cinerea in symptom- 
less strawberry flowers and fruit by growing the fungus from surface-sterilized 
pieces of tissue, especially tissue from the stem end of berries; 74% of isola- 
tion attempts from the stem end yielded B. cinerea, compared with 6% 
successful isolations from the distal portion of the berry. Powelson showed 
that a high proportion of necrotic flower parts (petals, stamens, and calyces) 
contained the fungus, and that when flower parts were removed after pollina- 
tion, the incidence of ripe fruit rot was considerably reduced under green- 
house conditions that favored the disease. Similarly, the application of captan 
three times during flowering significantly reduced the incidence of fruit rot in 
the field and the incidence of symptomless infection in marketable fruit. In- 
vasion of receptacle tissue usually occurs by growth of the mycelium inter- 
nally. 

Jarvis (1962a) confirmed that these quiescent infections occur in straw- 
berries and showed that they also occurred in raspberries and (Jarvis, un- 
published) in black currants. The occurrence of B. cinerea was greatest in 
floral parts that had been slightly damaged by frost. The period between 
flower infection and the appearance of fruit rot may be as long as 5 or 6 
weeks, but the onset of symptoms can be accelerated in very wet weather to 
appear, unusually, in unripe green fruit. Often the rot does not appear until 
after the fruit is picked, and its appearance may well depend on conditions of 
storage and marketing, although there is little information on this. 

Jarvis and Borecka (1968) established a correlation between the inci- 
dence of blossom blight and latent infections in strawberry flowers resulting 
in fruit rot. Flower susceptibility to infection resulting in fruit rot, however, 
was not related to the rate of growth of the fungus in fruit tissue but the 
incidence of calyx and total flower lesions was related to the growth of the 
fungus through fruit tissue from a spore inoculum. 

The presence of latent infections in grape flowers was also established 
by Natal'ina and Svetov (1972^), McClellan (1972), McClellan and Hewitt 
(1973), and McClellan, Hewitt, La Vine and Kissler (1973). In California, 
B. cinerea infects the stylar end of the flower and becomes latent in the ne- 
crotic stigma and style tissue. Later, as the berry develops, the fungus may 
become aggressive and rot it in mid-season, despite the absence of the rain 
normally associated with late-season grape rots. 

Wilson (1963) found a quiescent condition in the glasshouse tomato 
stem rot disease caused by B. cinerea. Here, lesions are usually found at the 
sites of deleafing scars left after the removal of senescent lower leaves in the 
early part of the growing season, but there is often a long delay between 
deleafing and aggressive development of the fungus, sometimes up to 12 
weeks (see PART 4, "Infection"). 

105 



The incubation period varied with the age of the plant at inoculation and 
with the position of the inoculated node on the stem; the younger the plant 
and the higher the node (and hence the younger the tissue), the longer the 
period. 

Tichelaar (1967) found that B. allii is able to attack young onion plants 
without impeding their growth. Using radioactive phosphorus as a label for 
conidia, he showed that the mycelium in the leaves is at first restricted to 
the colorless epidermal cells and that the infection remains symptomless. As 
the leaves age, the mycelium penetrates the adjoining leaf parenchyma and 
grows down into the neck of the bulb. The presence of the fungus in symptom- 
less bulbs can be demonstrated by treatment with methyl red because invaded 
tissue has an acid reaction of pH 4.2 compared with pH 6.6 for healthy tis- 
sue. The reaction zone extends for about 1 cm beyond the hyphae. The 
characteristic neck-rot symptoms caused by B. allii were rarely found in the 
field in the Netherlands, but appeared in storage, evidently as a development 
of this symptomless mycelium. Tichelaar found plants of all ages to be 
susceptible to infection, older plants being slightly more susceptible, and the 
fungus was detected in bulbs 4-7 wk after leaf inoculation. 

Jarvis (unpublished) believes that there may be a similar symptomless 
growth of B. narcissicola down beheaded flower stalks to the Narcissus bulb, 
and the situation may be comparable in onions where the brown stain disease 
caused by B. cinerea appears on previously symptomless bulbs in storage 
(Clark and Lorbeer 1973«, 19736). 

The tomato fruit ghost spot disease caused by B. cinerea (Read 1936; 
Ainsworth, Oyler, and Read 1938; Darby 1955; Owen and Ferrer 1957; and 
Ferrer and Owen 1959) was considered by Verhoeff (1970) to be a case of 
latent infection. Like previous workers, he could find no mycelium in the 
necrotic cells by any of the histological methods he used, although he was 
able, for the first time, to re-isolate the fungus. He concluded that despite the 
apparent failure of the fungus ever to develop further in the fruit, ghost spot 
represented a latent condition, or more correctly, a quiescent infection. 

Little is known of the factors maintaining the equilibrium of the host- 
parasite combination in a quiescent state or of the changes permitting the 
fungus to become aggressive (Verhoeff 1974), although Thatcher (1939, 1942) 
put forward a hypothesis in terms of increasing host cell permeability and the 
relative osmotic pressures of host and parasite cells (see PART 4, "Patho- 
genesis"), which could apply in this case. 

There is some circumstantial evidence that water content of the affected 
tissues may be one of the determining factors. Jarvis (1963) noted that heavy 
rain after a long dry period resulted in an increase from 86.8 to 90.1% in the 
water content of strawberry fruits. This effect, simulated by supplying water 
via a cotton wick threaded through the pedicel of strawberry and raspberry 
fruits, in all cases accelerated the onset of the quiescent-aggressive transition 
of B. cinerea. In six raspberry cultivars, the volume of the concavity at 
the top of the receptacle, which could perhaps be regarded as a water-holding 

106 



container, was correlated with susceptibility to B. cinerea. Similarly, the 
appearance of fruit rot from the stem end in wet fruiting seasons may re- 
present early development of latent infections (Jarvis 1964). 

Wilson (1964) advanced the onset of the transition of B. cinerea in 
tomato stems by irrigation, as compared with that in plants held just above 
the wilting point. 

Temperature changes may affect the termination of latency; for ex- 
ample, Vanev (1966) found the incubation period in grapes to be temperature- 
dependent. Stevens (1919) and Stevens and Wilcox (1920) noted that the 
temperatures of various small fruits when picked were as much as 8°C or 
10°C higher than ambient temperature, especially if the fruits were isolated. 
Physiological changes induced by picking may affect the course of latency, 
although there is no evidence on this point. 

Results that may be interpreted in part as early onset of aggression 
occurred in stem rot {B. cinerea) on tomatoes grown in soils of relatively low 
nitrogen status (45 ppm) (Verhoeff 1968). In soils with more nitrogen (165 
ppm) there were fewer stem lesions at a given stage of crop development and 
the plants were in a more vigorous vegetative state. This effect seems to be 
one of delayed aging or senescence. 

The transition usually occurs in older tissues, and the determining 
mechanisms, like some of those of general susceptibility, and aggressive and 
nonaggressive lesions, may well be connected with physiologic processes of 
aging and senescence, which are more fully discussed in PART 4, "Resis- 
tance". 



Implications of quiescence in disease control 

Disease control measures can be directed against quiescent infection in 
two ways: (i) chemical prophylaxis may be timed so that fungicides are 
brought into contact with newly alighting conidia or with germ tubes and (ii) 
crops may be manipulated to retard the quiescent-aggressive transition to a 
point at which yield is least affected. 

An example of the first approach is the retiming of fungicide programs, 
which has brought considerable benefit in raspberry and strawberry crops 
(Jarvis 1966^; Borecka 1967). However, the precise stages in flowering at 
which to spray are difficult to define because of the long sequence of flower 
development on the cymose inflorescences and because of the considerable 
variation between cuhivars, localities and seasons (Jarvis 1969). Similarly, 
bloom-time application of captan and early bloom-time applications of be- 
nomyl were effective in controlling early Botrytis rot in grapes (McClellan et 
al. 1973). Attempts to control tomato stem rot by applying fungicides at 
deleafing have not been successful (Wilson 1963), probably because fungi- 
cides are sucked past the spores in vessels, but the systemic fungicide benomyl 
has proved more successful (Fordyce 1969). 

107 



In the second approach, over-irrigation of soft fruit and tomatoes would 
appear to be a predisposing factor (Jarvis 1963; Wilson 1963) and, in toma- 
toes, the provision of adequate nitrogen to the soil delays the appearance of 
stem lesions (Verhoeff 1968). 

In picked strawberries and raspberries, avoiding high storage tempera- 
tures, including those resulting from insolation, delays the appearance of fruit 
rot. Stevens (1919) and Stevens and Wilcox (1920) showed that the temper- 
ature in picked small fruits exposed to direct sunlight could be as much as 
8°C to 10°C higher than the ambient temperature, and that the incidence of 
gray mold in the market was higher in insolated fruit than in shaded and 
cooled fruit. They stressed the value of removing 'field heat' and Harvey and 
Pentzer (1960) among many others have discussed the merits of refrigerated 
transport in disease control. 

Preharvest fungicides have also been shown to reduce storage losses in 
strawberries (Gilles 1964; Jordan 1973; among others), in raspberries (Mason 
1973), and in grapes (Harvey 1955^; McClellan, Hewitt, La Vine, and 
Kissler 1973). 



DISEASE ESCAPE 



Some plants and tissues have an intrinsic resistance to Botryds spp., for 
example, peanut cultivars (Alexander and Boush 1964), strawberry cultivars 
(Barritt, Torre, and Schwartze 1971; Barritt 1972; Kolbe 1971; Priedite and 
Ozohna 1971; and Naumova 1972), raspberry cultivars (Barritt 1971; Kolbe 
1973; and Mel'nikova 1972), as well as lettuce cultivars to B. cinerea (Ogil- 
vie and Croxall 1942), and onions to B. squamosa (Bergquist and Lorbeer 
1971). Such resistance, however, is never absolute and is most likely of the 
polygenic type. 

Brown, in his review (1934), points out the desirability of using various 
disease-escape mechanisms as adjuncts to chemical control. Some plants have 
a habit that reduces the likelihood of infection. Darrow (1966) noted that 
firm-fruited strawberry cultivars were less susceptible to B. cinerea than soft- 
fruited cultivars, as were those with less dense foliage, although their exposed 
early flowers were more susceptible to frost damage. Hughes (1965«, 1965/?) 
also commented on the adverse effects of dense foliage. Esmarch (1926) sug- 
gested that strawberry cultivars with long stiff inflorescences, holding flowers 
and fruit clear of the foliage canopy, would be less susceptible to B. cinerea, 
and indeed, Koch (1963) bred such a cultivar. Tompkins (1950) noted that 
Begonia cultivars with red flowers and hairy stems were more resistant to 
B. cinerea than cultivars with light-colored flowers and smooth stems. A 
similar observation was made by Jennings (1962) and Knight (1962) in the 
case of raspberry canes; the more resistant cultivars had relatively hairy, 

108 



spineless, waxy and nonpigmented canes, and Jennings attributed escape, 
at least in part, to a greater runoff of surface water. 

Nelson (1949) found the compactness of the fruit bunch to be important 
in the susceptibility of grapes; the looser bunches had less crushing damage 
and B. cinerea spread less rapidly from berry to berry by direct growth. 
Jarvis (1962^) found this also to be true in strawberries and raspberries, 
where the length of the peduncle as a path for mycelial growth was also 
probably important in berry-to-berry spread. 

Thomas and Orellana (1963^) also found the structure of the flower 
raceme of castor bean to be important in its susceptibility to B. ricini; com- 
pact inflorescences were more severely attacked than loose inflorescenses, and 
staminate flowers were very susceptible, as were cultivars with short inter- 
nodes. The presence of a waxy bloom appeared to offer little protection. The 
compact inflorescences and short internodes favored surface water retention 
and hence improved the likelihood of infection. Strawberry cultivars with 
staminate flowers are also more susceptible to B. cinerea (Risser 1964). Fur- 
ther, Lemaitre (personal communication) noted that strawberries that become 
red before attaining their maximum volume are generally less susceptible than 
those that redden late, and they also tend to be firmer. Lemaitre also thought 
that strawberries having a marked neck with the calyx raised clear of a convex 
receptable, those with superficial rather than sunken achenes, and those with 
readily falling petals were all less susceptible to gray mold. 

Inflorescence habit can be manipulated to some extent (Vidal 1962; 
Vidal, Nebout, and Cattoen-Vidal 1963). Weaver, Kasimatis, and McCune 
(1962) sprayed developing inflorescences of grapes with a gibberellin, and 
Jarvis (1963) similarly sprayed those of raspberries; treated pedicels were 
appreciably longer, the fruit bunches therefore looser, and there was less gray 
mold. 

Abdel-Salem (1934) and Brown (1934) attributed the differences in 
susceptibility to B. cinerea of two lettuce types, cos and cabbage, to their 
different growth habits; the cos type was much less attacked in summer, 
though both were equally susceptible as seedlings. 

The speed with which tissues attain maturity, as opposed to senescence, 
may also be of importance in disease escape, especially in lignifying tissues. 
Thus, Lamberti (1965) found that early-ripening grape cultivars were less 
susceptible to B. cinerea than late-ripening cultivars. 

There are many ways in which crop management techniques may be 
modified to promote disease escape: Brown and Montgomery (1948) planted 
lettuce on ridges and in hollows; the plants on the ridges had a greater inci- 
dence of gray mold because, it was suggested, they were predisposed by 
greater frost damage. Criiger (1962) discussed the ways of manipulating the 
glasshouse environment to avoid gray mold in lettuce. Similarly, Schellenberg 
(1955) reviewed the problem in vineyards. 

109 



The predisposing effect of dense plant spacing is frequently recorded 
in the literature. There is the additional effect of an accumulating inoculum 
on crop debris, for example, in Douglas fir seedlings (Halber 1963) and in 
flax (van der Spek 1960). The situation is also aggravated by the presence of 
weeds, which serve as hosts for B. cinerea (Wormald 1942) and induce a 
microclimate favoring infection (Robinson 1964). Campbell (1949) found 
that, in addition to density of plantings of beans, row orientation with respect 
to the prevailing wind had an effect, because he noted more gray mold in 
rows at right angles to the wind. Wilson (1937) noted a similar pattern in the 
incidence of chocolate spot, and Kovacs (1969) observed that strawberries 
protected from the prevailing wind by a hedge, 4 m high, had almost twice 
as much gray mold as plants 40 m away from the hedge. Jarvis (1961), how- 
ever, could not explain the uneven distribution of gray mold in a raspberry 
plantation in terms of wind direction. 

Vyskvarko, Mikhailyuk, Pliss, Vaselashku, Vasilaki, and Yuresko (1971) 
succeeded in reducing the incidence of gray mold on grapes by removing 
some of the leaves with a magnesium chlorate spray. 

Deep planting can predispose plants to infection as occurred in Gerbera 
(Garthwaite 1963), but in Begonia semperflorens the promotion of active 
adventitious rooting by the use of long-day cultivation compensated for the 
loss of main roots attacked by B. cinerea (Sironval 1951). 

In poorly managed glasshouses where ventilation is restricted, crops are 
particularly susceptible to infection by B. cinerea, and control of gray mold 
then becomes largely a matter of manipulating ventilation efficiently (Criiger 
1962; Wilson 1963; and Winspear, Postlethwaite, and Cotton 1970). 

The rate of fungal growth relative to the speed of the host's defence reac- 
tion offers a means of manipulating the environment in favor of the host. 
Controlling temperature is the simplest and most usual way, for example, cool 
storage; controlling the atmosphere is another simple way (Harvey and 
Pentzer 1960; Haas and Wennemuth 1962; and Redit 1969). Temperature 
control was shown by McColloch and Wright (1966) to be important in 
avoiding rot by B. cinerea in stored bell peppers. The decay of wound- 
inoculated peppers and the rate of fungal growth in vitro generally increased 
with temperature in the range 0-21 °C, but more decay occurred at 10°C 
than at 13°C. Naturally infected peppers decayed fastest at 4°C; little rot 
occurred at 10°C and 13°C. Peppers, prestored at 0°C and then spore- 
inoculated and transferred to 55 °C, rotted at rates proportional to the dura- 
tion of their stay at 0°C. 

In certain bulb diseases, including those of Allium spp., the success 
of infection of the emerging shoot from mycelium established in the neck 
probably also depends on the relative growth rates of the fungus and shoot. 
The shoot of tulip (Price 1967), narcissus (Jarvis unpubUshed), and onion 
(Tichelaar 1967) may become infected in this way when the tip is still in the 
neck or at any point along its length or it may escape infection if the fungus 

110 



fails to grow fast enough through scale leaf tissue. The relative growth rate 
must be determined by many edaphic, nutritional, and meteorological factors. 

On a different scale, respective activities of pathogen and host at different 
times of the year offer opportunities to manipulate crops for disease escape. 

In the chocolate spot disease (B. fabae) of beans, Grainger (1950) found 
that, although the vegetative growth of bean plants became susceptible to 
B. fabae after July, the disease had little effect on bean yield. Most of the 
dry weight of the seeds was already laid down by July and subsequent vegeta- 
tive growth was of little value in crop production. Chocolate spot, therefore, 
limited yield only in years when B. fabae appeared early. 

A disease of flax caused by a fungus cited as Botryds lini (B. cinerea), 
however, behaved in the opposite way and was more prevalent on flax in 
years when chocolate spot was low. This disease did not have much effect on 
yield either, because the increased vigor of unaffected, competing stems com- 
pensated for the stems killed by B. lini. 

Alekseeva and Taov (1971) reduced the incidence of gray mold on 
sunflower by altering the sowing time and removing infected plants at flower- 
ing, and Wilson (1937) also indicated the possibility of avoiding epiphytotics 
of chocolate spot of beans by sowing in the spring rather than the autumn. 

Howard and Horsfall (1959) reported that the removal of fruits and suc- 
culent cane tips of rose bushes prevented the advance of B. cinerea down- 
wards through the pith and into the crown. 

In an unusual case, the induction of abscission in tomato leaf petioles 
caused by B. cinerea has been exploited as a disease-escape mechanism by 
Verhoeff (1967). Leaving somewhat longer petiole stubs than is usual in 
commercial practice, and inoculating them deliberately, Verhoeff succeeded 
in hastening their abscission to leave a healed scar with the minimum of 
necrotic tissue that might act as a possible saprophytic base. 



EPIDEMIOLOGY 



Epiphytotics caused by Botrytis spp. are generally associated with cool, 
wet, and humid weather, conditions favoring sporulation and infection and 
possibly also having an adverse effect on the host. These conditions are 
described in general terms by Anderson (1924), Heald and Dana (1924), 
Foister (1935), and Baker (1946). The conditions for epiphytotics in some 
other crops are discussed in these papers: 

Grapes Stalder (1953a), Bouard, Bulit, Lafon and 

Roussel (1970), Ciccarone (1970), Bulit and 
Lafon (1970, 1972), Gartel (1969, 1970, 1971), 
and Lehoczky (1972) 

111 



Strawberries Rose (1926), Stolze (1962), Devaux (1970), 

Kolbe (1970, 1973), Fulton (1956), and Jordan 
and Hunter (1972) 

Raspberries Fulton (1956) 

Figs Ricci(1972) 

Glasshouse crops Bewley (1923), Kadow, Anderson, and Hop- 

perstead (1938), and Ogilvie and Croxall (1942) 

Onions Jones (1944), Beraha (1968), and Kaufman, 

Lorbeer, and Friedman (1964) 

Peas Ford and Haglund (1963) 

Beans Berger (1937), Yu (1945), Bremer (1954), 

Sirry, Ashour, and Hegazi (1966), Gerlach and 
Rudnick (1972), and Sundheim (1973) 

Tobacco Wolf (1931) 

Kenaf Withers (1973) 

Flax van derSpek (1965) 

Tulips Valaskova (1963) 

Ornamental bulb crops Moore (1949) 

There are also more precisely described conditions promoting and limit- 
ing the spread of the gray mold diseases. Hunter and Rohrbach (1969) and 
Hunter, Rohrbach, and Kunimoto (1972) found a correlation between the 
incidence of B. cinerea on Macadamia racemes and the number of hours 
per week the leaves remained wet at temperatures between 18°C and 22 °C. 
Bakos, Bekesi, and Szurke (1939) found a correlation between the incidence 
of B. cinerea on sunflower and rainfall; Wilson (1937) between the incidence 
of chocolate spot (B. fabae) on beans and heavy rainfall from April to July; 
Hogg (1956) between chocolate spot and the frequency of hours in which 
the relative humidity exceeded 95%; and Grainger (1950) between chocolate 
spot and the h/wk of saturation; McClellan, Baker, and Gould (1949) the 
relation between temperature and humidity and B. gladioli on Gladiolus; 
Page (1955), Lutynska (1968), and Shoemaker and Lorbeer (1971) the 
relation of rainfall, relative humidity, temperature, and light to onion dis- 
eases; Nelson (19516), Stellwaag-Kittler (1969), Krumov (1969), and Bulit, 
Lafon, and Guillier (1970) the relation of relative humidity and the number 
of wet days in late summer to grape gray mold; Hennebert and Gilles (1958) 
and Gilles (1959) the relation of strawberry gray mold to relative humidity, 
surface wetness and temperature, and Hughes (1965/?) its relation to irriga- 
tion. All of these factors act differentially in strawberries, raspberries, and 
grapes that are insolated and in those that are shaded and sheltered (Jarvis 
1961; Kovacs 1969, Lehoczky 1972; and Lafon 1974). 

The delicate balance in water relations determining whether grapes are 
rotted by the pourriture noble or by the pourriture grise is discussed by 

112 



Ribereau-Gayon (1970), Seguin (1973), and Lehoczky (1972); see also 
PART 4, "Enology". 



Forecasting 

There have been relatively few attempts, using meteorological data, to 
forecast epiphytotics either in the field or in storage (Large 1955). Large em- 
phasized the need to consider all aspects of the life cycle of the parasite, 
citing B. tulipae, the cause of tulip fire, as an example. Jarvis (1964) estab- 
lished a correlation as much as 30 days before harvesting began between the 
incidence of gray mold in strawberries and high rainfall and the duration of 
relative humidities exceeding 80% during flowering. In raspberries there was 
a similar correlation with weather conditions in the 5-day period immediately 
before harvesting, and also with conditions during harvesting; the interval 
between individual harvests was important — the longer the interval, usually 
because of bad weather, the more gray mold at the next harvest. 

Herve and Moysan (1967) found an empirical, graphical method of fore- 
casting the incidence of gray mold in strawberries; they plotted the number 
of hours per day when the relative humidity exceeded 90% (ordinate), 
against time (abscissa). On the same graph, and with the same numerical 
scale for h and °C on the ordinate axis, they also plotted the mean daily 
temperature against time, again on its same scale. Epiphytotics usually 
followed when the two curves intersected at least three times within 48 h 
in the ordinate range 14-16. Some flexibility in interpretation was neces- 
sary; infection occurred when RH was consistently high and the temperature 
below 18°C (though the curves did not then intersect), and 25 °C was the 
maximum temperature. 

Jarvis (1964) considered that forecasting was probably very difficult 
because of the complex effects of many meteorological, edaphic, and biotic 
factors on host, parasite, and the host-parasite combination. The conditions 
affecting infection from conidia are different from those affecting infection 
from colonized substrates, from those affecting spore dispersal (another 
method of forecasting considered but rejected by Jarvis (1962a, 1962/?)), 
and from those affecting the behavior of latent infections. Although in the 
case of strawberries and raspberries, a forecasting method could indicate the 
necessity of frequent harvesting and careful storage, it could not help in the 
correct timing of prophylactic fungicide applications. Infection occurs so 
rapidly (Hennebert and Gilles 1958; Gilles, 1959) that a mycelium, either 
latent or aggressive, could be established before the end of the minimum 
24-h observation period (Herve and Moysan 1967). Bulit, Lafon, and Guil- 
lier (1970) found infection of grapes by B. cinerea to occur when the grapes 
remained wet for 15 consecutive hours at 15-20°C and they suggested that 
control measures should then be applied, but again, with this hindsight, it 
is doubtful whether standard prophylactic fungicide sprays would then be 
effective. 

113 



Harvey (1955fl) developed a method of forecasting the incidence of 
gray mold in stored grapes. He established a very close correlation in grapes 
surface-sterilized with 1 % sulfur dioxide (a standard commercial practice) 
between the proportion of a sample that rotted at room temperature within 
10 days and the proportion rotting of the bulk of the grapes stored at about 
0°C for 10-16 wk. 



INTERACTION WITH OTHER MICROORGANISMS 



Evidence on the role of Botrytis cinerea in controlling the parasitic 
activity of other microorganisms is sparse and conflicting. Broadfoot (1933) 
found B. cinerea to limit the pathogenicity of Gaeumannomyces graminis 
and to be antagonistic to it on potato dextrose agar, but Lai (1939) could 
find no such activity. Savastano and Fawcett (1929) found that B. cinerea 
depressed the rate of decay of citrus fruits caused by Penicillium italicum 
and P. digitatum at 9-1 8°C but at 22-30°C all three fungi together rotted 
lemons faster than each alone. 

B. alia (B. aclada) markedly interfered with the parasitic activity of 
Monilia fructigena when spores of both fungi were mixed in the inoculum 
for apple fruits; Vasudeva (1930/?) explained this interference by postulating 
that staling products of B. allii in the infection drop inhibited the growth of 
M. fructigena. 

In mixed inocula with Nectria cinnabarina, the activity of B. cinerea on 
Prunus domestica varied with the time of year (Mostafa 1941a, 1941 b). In 
February, the pathogenicity of B. cinerea was enhanced, in April it was 
decreased, and in December, January, and March, the presence of B. cinerea 
increased the parasitic activity of N. cinnabarina. Interaction occurred both 
in the infection drop and in the host. B. cinerea and Stereum purpureum were 
mutually inhibitory. 

Also in mixed inocula, B. cinerea reduced the parasitic activity of 
Pythium debaryanum on Fuchsia sp. pistils and was strongly antagonistic 
to it in culture (Schonbeck and Schinzer 1970), but this report contrasts with 
the synergistic effect of these two organisms on lettuce noted by Basile 
(1952). Fehlhaber et al. (1974) later characterized the antibiotic botrydial 
from culture filtrates of Schonbeck's isolate as a sesquiterpene. 

Purkayastha (1966) mixed equal numbers of conidia of B. fabae and 
B. cinerea in inocula for bean leaves, and found no significant difference in 
the numbers of spreading lesions caused by B. fabae alone, and by both 
fungi together. When there were twice as many conidia of B. cinerea as of 
B. fabae in the inoculum, there were no spreading lesions typical of B. fabae, 
and Purkayastha suggested that antifungal substances were produced in the 
lesion area, as had been postulated earlier (Purkayastha and Deverall 1964). 

114 



B. cinerea was shown to be very sensitive to Trichothecium spp. (Sido- 
rova 1954) and Botrytis sp. to Trichoderma spp. (Matsumoto 1939; Yama- 
moto 1954; Likhachev and Vasin 1970; and Wells, Bell, and Jaworski 1972). 
The mycelial growth of B. cinerea was found by Ale-Agha, Dubos, Gros- 
claude, and Ricard (1974) to be inhibited by heat-killed spores of Tricho- 
derma viride at a concentration of lO'^'-lO^ spores/ml but only in the presence 
of ascorbic acid at 2 mg/litre, which lowered the pH to 3.1. 

The growth of germ tubes of B. cinerea was inhibited by bacteria on 
the surface of Chrysanthemum and beetroot leaves; the effect was greater 
on older leaves and was reversed by removing the bacteria by various means 
(Blakeman and Fraser 1971; Blakeman 1973; Sztejnberg and Blakeman 
1973a, 1973^; and Blakeman and Sztejnberg 1974). It was suggested that 
the epiphytic bacteria play some part in the resistance of Chrysanthemum; 
this resistance is more correctly called disease escape. Subsequent work by 
Sztejnberg and Blakeman (1973^) suggested that bacteria with copious poly- 
saccharide sheaths could act as sinks for nutrients on beetroot leaves, so 
that spores of B. cinerea were unable to germinate there, an effect simulated 
by leaching nutrients from spores in vitro. It seems likely that this is a com- 
mon phenomenom; B. cinerea and probably other species are common in 
the phyllosphere (e.g., Kerling 1964; Holloman 1967; Skidmore and Dick- 
inson 1973; and Godfrey 1974), but never attack healthy leaves. 

Kadymova (1971) also noted that certain bacteria and their culture 
filtrates, because they were antagonistic to B. cinerea, gave some control 
of B. cinerea on grapevine, and Cleary (1959) attributed the comparative 
absence of gray mold in lettuce affected by bacterial wilt to the antagonism 
of the bacterial pathogen Pseudomonas marginalis. 

Ujevic, Kovacikova, and Urosevic (1970) found a number of bacteria 
and fungi antagonistic to B. cinerea, especially Fusarium oxysporum, and 
Penicillium expansum reduced the incidence of gray mold in young lentil 
plants. 

The control of plant diseases by the use of antagonistic organisms has 
always been of interest (Wood and Tveit 1955) and the first gray mold disease 
to be investigated in this context was that of lettuce caused by B. cinerea 
(Asthana 1936; Newhook 1951^, 1951^; and Wood 1951). Many organisms 
that were antagonistic in vitro, including T. lignorum and a Phoma sp. and 
several bacteria, prevented pathogenesis by B. cinerea if they were first inoc- 
ulated onto lesions simulating frost damage. Control was particularly effec- 
tive at high temperatures but not so effective at the normal temperature of 
lettuce cultivation. B. cinerea was unable to colonize tissues already colonized 
by certain other organisms. Some control of B. cinerea in field conditions was 
obtained by spraying lettuce seedlings with antagonists in 1% glucose solu- 
tion, but control under commercial conditions was unsuccessful. Nevertheless, 
prior colonization of necrotic tissues by antagonists probably accounts for 
some disease escape from B. cinerea in field conditions. 

Newhook (1957) also found that colonization of dead tomato petals by 
B. cinerea was prevented by prior colonization by species of Cladosporium, 

115 



Penicillium, and Alternaria; when petals adhering to fruit surfaces after the 
appHcation of fruit setting sprays were so colonized, the incidence of B. 
cinerea on them was reduced by 30-100% . 

Similarly, Bhatt (1962) and Bhatt and Vaughan (1963) were able to 
reduce the colonization of strawberry flower parts by prior inoculation by 
Cladosporium herbarum; and Voznyakovskaya and Shirokov (1961), Musli- 
mov (1965), and Jouan and Lemaire (1971) reduced it with various bacteria. 

Sometimes, severe attacks by Botrytis spp. are observed after soil 
sterilization; these attacks have been attributed to the absence of competitive 
or antagonistic microorganisms. For example, Behr (1966) noted one in flax 
and MacWithey (1967) one in Iris rhizomes invaded by B. convoluta. B. 
cinerea seemed to be controlled in soil by Trichoderma koningi, the inhibitory 
effect of which increased with pH (Schuepp and Frei 1969). In contrast, 
Ale-Agha, Dubos, Grosclaude, and Ricard (1974) found that in vitro inhibi- 
tion by dead spores of T. viride is enhanced by ascorbic acid at pH 3.1. 

The degradation of sclerotia in soil as a method of reducing the inocu- 
lum levels of B. cinerea has been reported by Pohjakallio, Salonen, Ruokola, 
and Ikaheimo (1956), Pohjakallio and Makkonen (1957), Karhuvaara 
(1960), Makkonen and Pohjakallio (1960), and Ervio (1965). The parasitic 
organisms include Acrostalagmus roseus (V erticillium roseum), Trichoderma 
viride, Trichothecium roseum, Coniothyrium minitans, Rhizopus nigricans, 
Sporotrichum carnis, and species of Verticillium, Penicillium, and Mucor. 

Gall midge larvae, nematodes, and mites were also found to destroy 
sclerotia of B. cinerea on stored grapevine grafted material (Cartel and Hering 
1965); indeed the midge larvae failed to spread in the absence of the fungus. 

Harrison (1952) found a species of the mite Pediculopsis that dispersed 
spores of B. gladiolorum among plants of Acidanthera and Gladiolus, and that 
was unable to establish colonies in the absence of the fungus. 



ENOLOGY 



As a pathogen of grapevines and grape berries, Botrytis cinerea is an 
extremely important organism and its epidemiology on this host has been 
reviewed by Schellenberg (1955), Bouard, Bulit, Lafon, and Roussel (1970), 
Bulit and Lafon (1970, 1972), Ciccarone (1970), Cartel (1967, 1969, 1970, 
1971), and Lehoczsky (1972). In addition, B. cinerea has profound effects on 
the quality of wine. Either the berries rot rapidly and completely, or, in 
suitable conditions, they decay very slowly permitting them to dry consider- 
ably; such dry grapes are made into the valuable and distinctively flavored, 
sweet wines such as the Sauternes of France, the Trockenbeerenauslese of 
Cermany, and the Aszu of Hungary. The destructive rot is known as pourri- 

116 



ture grise in France and Graufaule in Germany, and the 'noble rot' is the 
pourriture noble of France and Edelfaule of Germany. 

Grapes affected by the destructive rot are of no value for making wine; 
if they are included in the must, they impart a taint that can be counteracted, 
however, by the addition of sulfuric acid (Mathieu 1924). As a contaminant 
of wine cellars, B. cinerea also causes a taint (Mathieu 1929) and interferes 
with fermentation (Le Roux, Eschenbruch, and de Bruin 1973) by the produc- 
tion of a toxin complex, botryticine (Ribereau-Gayon, Peynaud, Lafourcade, 
and Charpentie 1955). It also decreases the coloration of red wines (Toth 
1971) and spoils wine quality (Flath, Forrey, and King 1972). 

Muller-Thurgau (1888) reported that grapes affected by noble rot lost 
about 25% of their weight, mostly as water, while their relative sugar content 
increased from 1 1.7% in mid-October to 19.6% by the end of November and 
their relative content of total acids from 17.4 to 22.1%. Despite the apparent 
rise in sugar content in the noble rot, the fungus did deplete them and at a 
faster rate and in relatively greater amounts than the loss of organic acids. 

Similarly Moser (1967) found that sugars were utilized in grapes affected 
by the noble rot, but in vintage years the sugar content was initially so high 
that not enough sugar depleted before the grapes dried out to impair the 
sweetness of the wine. 

The metabolism of grape constituents by B. cinerea has been studied by 
Stalder (1954), Ribereau-Gayon (1960, 1970), Ribereau-Gayon, Peynaud, 
Lafourcade, and Charpentie (1955), Sutidze (1962), Hofmann (1968), Nelson 
and Amerine (1956), de Jong, King, and Boyle (1968), Novak (1958), Novak 
and Voros-Felkai (1958), Dittrich (1964), and Champagnol (1969) among 
others; see also PART 3, "Metabolism". Tartaric and malic acids are both 
utilized (tartaric acid more so in vitro) as well as mono- and disaccharides, 
starch, cellulose and some glycosides, to yield glycerol, mannitol, and ethanol; 
gluconic, citric, acetic, succinic, glycolic, and lactic acids; and soluble dex- 
trans, using the enzymes glucose oxidase, laccase, tyrosinase, ascorbic acid 
oxidase, pectinases, and proteinase. Sutidze (1962) found tannins to be 
utilized and the must content to be reduced by as much as 77%. Jako and 
Nyerges (1967) also found the sugar content of infected grapevines to be 
decreased. Musts containing B. cinerea ferment very slowly. Ribereau-Gayon 
et al. attributed this slowness to the inhibition of yeasts by a complex of 2 
inhibitors; the pair are collectively termed botryticine and are destroyed by 
sulfuric anhydride or heat. 

The reasons why one vineyard may have the noble rot and its neighbor 
the destructive rot are not well understood (Ribereau-Gayon 1960). Dubos 
(personal communication) obtained no evidence that different races of the 
fungus are involved, although she did obtain evidence of differential patho- 
genicity of isolates from different parts of France. Pesante (1947) found some 
differences in the composition of musts attributable to different isolates of 
B. cinerea, while Saponaro (1953) merely found some morphological differ- 
ences between vineyard isolates. 

117 



Ribereau-Gayon (1960, 1970) found that must from healthy grapes from 
a destructive rot vineyard had twice the total N and ammonium N content of 
healthy grapes from a neighboring vineyard that had the noble rot. He (1960) 
also attributed the resistance of the cultivar St. Emilion to its very low N 
content. 

In both lots of grapes, 75-90% of this N disappeared when they were 
parasitized by B. cinerea. He concluded that the N nutrition of the grapevines 
has a profound effect on whether the rot is noble or destructive. Noble rot 
vineyards tend to be on nutrient-poor, well-drained, limestone soils; the plants 
are deep rooted and have a constant water supply that tends to decrease at 
fruit maturation. By contrast, vines on richer soils have more superficial roots 
and a widely fluctuating water supply; their fruits mature earlier and are more 
susceptible to cracking (Seguin, Compagnon, and Ribereau-Gayon 1969). 
Ribereau-Gayon (1960) also found that in the noble rot of Semillon grapes, 
22% of sugars were utilized, together with 49% of the tartaric acid and 8% 
of the malic acid; in the destructive rot of the same cultivar, 52% of the 
sugars were utilized, 44% of the tartaric acid, and 28% of the malic acid. 
In the noble rot of Sauvignon grapes the utilization of sugars, tartaric, and 
malic acids respectively was 27%, 40%, and 40%, compared with 36%, 
27%, and 24% for the destructive rot. The utilization of acids was relatively 
more important than that of sugars in the noble rot and the converse was 
true in the destructive rot. 

In California and Moldavia SSR, attempts have been made to reproduce 
the effect of a noble rot in harvested grapes by Nelson and Amerine (1956), 
Nelson and Nightingale (1959), Nelson, Kosuge, and Nightingale (1963), de 
Soto, Nightingale, and Huber (1966), de Jong, King, and Boyle (1968), Flath, 
Forrey, and King (1972), and Trofimenko and Tikhonova (1972). This 
process is known as 'botrytization'; hence the verb 'to botrytize'. Mature 
grapes were sprayed with a suspension of spores of B. cinerea and incubated 
at 98-100% RH and 20°C for 1 day, then at 50-60% RH for 1 wk. The 
wine made from these grapes was very sweet, but there tended to be a marked 
taint and the yields were small. Promising attempts were also made to produce 
sweet wines by growing B. cinerea in sterile grape juice before fermentation 
and also by adding enzymes from B. cinerea. 



PRINCIPLES OF CONTROL 



Diseases caused by Botrytis can be controlled in many ways, yet they 
remain among the most economically serious diseases, both in the field and 
in stored and marketed products. All phases in the biology of the causal 
organisms must be considered in the design of prophylactic and therapeutic 
treatments, in the modifications of cultural practices, and in the selection 
of new cultivars (Wood 1961 ; Jarvis 1965). 

118 



Fungicides 

In general, fungicides are of value only as prophylactics, but because of 
the rapidity of infection from conidia, little warning of the likelihood of 
infection can be obtained from a knowledge of relevant meteorological fac- 
tors. Moreover, the conditions permitting infection to occur often do not 
permit fungicide applications to be made to field crops; and fungicides effec- 
tive against Botrytis spp. in vitro are often not effective in the field because 
the fungicides affect host metabolism, are tolerated by the fungi, or are applied 
at an incorrect time and place (Gilles 1964; Jarvis 1966^, 1969; MUller 1964; 
Brandes 1971; and Lafon, Verdu, and Bulit 1972). Because many crops 
become affected by Botrytis spp. just before harvest, attention must be given 
to the levels of fungicides that can be tolerated in foods and in grape must 
(Lamberti and Quacquarelli 1965), and to fungicide efficacy in controlling 
rots developing after harvest. These considerations have been studied in 
strawberries by Gilles (1964), Freeman (1965), Maas and Smith (1972), and 
Jordan (1973); in raspberries by Mason (1973); and in grapes by Harvey 
(1955^), McLellan (1972), and McClellan, Hewitt, La Vine, and Kissler 
(1973). Fungicide applications after harvest add considerably to the costs of 
production and often are detrimental to food quality. 



Storage diseases 

Postharvest rots caused by Botrytis spp. often outweigh field diseases in 
their economic effects, although in some respects they are more amenable to 
control by careful storage and marketing techniques and certain other treat- 
ments: controlled-temperature or controlled-atmosphere storage, pasteuriza- 
tion, irradiation, fumigation and vapor-phase fungicides, and delay of ripen- 
ing (Wright, Rose, and Whiteman 1954; Harvey and Pentzer 1960; Haas and 
Wennemuth 1962; Smith 1962; Smith, McCoUoch, and Friedman 1966; 
Sommer and Fortlage 1966; Spalding 1966; Shibabe, Ito, and lizuka 1967; 
Eckert and Sommer 1967; Hansen 1967; Lutz and Hardenburg 1968; Redit 
1969; Ceponis 1970; Ceponis, Kaufman, and Butterfield 1970; Sutton and 
Strachan 1971; Aharoni and Stadelbacher 1973; and Sommer, Fortlage, 
Mitchell, and Maxie 1973). There are also several ways of treating crops 
immediately pre- or post-harvest to ensure that they enter storage in good 
condition, for example, keeping produce from contact with saprophytically 
based inocula on the soil or on containers or in plant debris (Jarvis 1960«; 
Jenkins 1968), removing field heat by precooling (Duvokot 1965; Hall 1966; 
and Mitchell, Maxie, and Greathead 1964), and curing onions to dry out the 
neck before storage (Vaughan 1960; Harrow and Harris 1969; and Bottcher 
1973). 



Disease escape 

Considerable contributions to control may be made by various manipu- 
lations of environment and habit that confer disease escape and these can be 

119 



supplemented by modifications of cultural practices that confer resistance 
(e.g., liming in the case of tomato, lettuce, and strawberry gray mold) and by 
the selection of new cultivars. Cultural practices that predispose to infection 
(e.g., over-dense crops) should be avoided. Reductions in inoculum, both 
mycelial and conidial, can be achieved by attention to crop hygiene, that is, 
the removal of alternative weed hosts, perhaps aided by specific antisporulants 
such as tecnazene and hexachlor-2-propanol. 

Little attention has been paid to the practical possibilities of exploiting 
the degradation of sclerotia in or on the soil, although they are parasitized 
by many organisms; and the control of infection by prior colonization with 
other microorganisms has been shown to be feasible in certain circumstances. 

Little is known of the relative importance of conidia and ascospores in 
infection, but ascospores are probably of greater importance than has hith- 
erto been supposed. If they are important, then some attention to the biology 
of sclerotial germination, apothecial formation, ascospore discharge, and the 
inhibition of all of these processes could be rewarding. 



Breeding for resistance 

No major gene-resistance against Botrytis spp. is known; this is hardly 
surprising in view of the wide range of methods and the wide range of en- 
vironmental conditions in which these species can attack their hosts. One or 
two intrinsic resistance mechanisms are known and some features of habit 
conferring disease escape (q.v.), but relatively few diseases are the subject of 
special attention by plant breeders. The careful techniques elaborated by van 
der Meer, van Bennekom, and van der Giessen (1970) for screening Allium 
spp. for resistance to B. allii are an exception; these techniques take into 
account most aspects of infection and pathogenesis. Vasileva (1973) made a 
study of the inheritance of resistance to B. cinerea in an F^ generation of 
grapes. 



120 



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180 



APPENDIX 



Additional Literature 

These important references were noted since the text was drafted in 
December 1974, or were inadvertently omitted from it, or were not discussed 
there. To aid in assessing the coverage of these papers, each reference is fol- 
lowed by key words, set in italics. These key words are in line with the BOTBIB 
computer-filed bibliography on Botrytis and Botryotinia spp. that is compiled at 
the Scottish Horticultural Research Institute and filed at the Edinburgh Uni- 
versity Computer Centre (Jarvis and Topham: Bull. Br. Mycol. Soc. 8:37. 
1974). 



Aharoni, N., Haas, E., and Ben-Yehoshua, S. 1970. Effects of carbon dioxide and 
precooling on the keeping quality of strawberry fruit. Proc. 18th Hortic. Congr. 
1: 28. 
Fragaria Botrytis-cinerea carbon-dioxide storage refrigeration 

Ale-Agha, N., Dubos, B., Grosclaude, C, and Richard, J. L. 1974. Antagonism 
between nongerminated spores of Trichoderma viride and Botrytis cinerea, 
Monila laxa, Monila fructigena, and Phomposis viticola. Plant. Dis. Rep. 58: 
915-917. 
Botrytis-cinerea conidium germination antagonism 

Anselme, C, and Champion, R. 1975. Etude de la transmission du Botrytis cinerea 
par les semences de tournesol {Helianthus annuus). Seed Sci. Technol. 3: 
711-717. 
Helianthus Botrytis-cinerea seed-dispersal storage survival 

Balazs, K. 1975. A Botrytis cinerea Pers. es a termeshozam alakulasa kozotti 
osszefugges szamocan Novenyved Korzerusitese Novenyved Kut Intez. Kozl. 
8: 211-230. 
Fragaria Botrytis-cinerea predisposition water fertilizer quiescence 

Barkai-Golan, R., Aharoni, N., Dubitzky, E., and Sivan, J. 1974. Fungicide applica- 
tions to lettuce in the field to prevent diseases in storage. Hassadeh 55 : 497-501 . 
Lactuca Botrytis-cinerea quiescence storage fungicide control 

Bekker, Z. E., Asimova, R. M., and Pushkareva, I. D. 1975. (The effect of membrane- 
active substances and antibiotics with systemic action on Fusarium oxysporum 
Schlecht. f.sp. vasinfectum (Robin.) Berkh.) Mikol. Fitopatol. 9: 369-376. 
Botrytis-cinerea antibiotic antagonism 

Beran, F. 1974. Neue probleme in Weinbau. Winzer 30: 243-244. 
Vitis Botrytis-cinerea epidemiology 

Bergman, B. H. H., and Noordermeer, C. E. I. 1975. Leaf scorch and neck rot in 
narcissus. Acta Hortic. 47: 131-135. 
Narcissus Botrytis-narcissicola synergism storage control fungicide 

Beyma thoe Kingma, F. H. van. 1927. Uber eine Botrytis- An auf Rotkleesamen, 
Botrytis trifolii nov. spec. Meded. Phytopathol. Lab. W. C. Scholten 10: 37-42. 
Botrytis-trifolii taxonomy 

181 



Beyma thoe Kingma, F. H. van. 1927. Uber eine neue Sclerotinia-An auf Porreesa- 
men (Allium porrum), Sclerotinia porri nov. spec. Meded. Phytopathol. Lab. 
W. C. Scholten 10: 42-46. 
Botryotinia-porri taxonomy 

Beyma thoe Kingma, F. H. van. 1927. Die Botrytis-Kvdir\k\\Q\X der Paeonien. Meded. 
Phytopathol. Lab. W. C. Scholten 1 1 : 60-66. 
Botrytis-paeoniae taxonomy 

Black, R. L. B., and Dix, N. J. 1976. Spore germination and germ hyphal growth of 
microfungi from litter and soil in the presence of ferulic acid. Trans. Br. Mycol. 
Soc. 66: 305-311. 
Botrytis-cinerea phenolic conidium germination growth soil 

Black, R. L. B., and Dix, N. J. 1976. Utilization of ferulic acid by microfungi from 
litter and soil. Trans. Br. Mycol. Soc. 66 : 313-317. 
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